Factors restraining the population growth of Varroa destructor in Ethiopian honey bees (Apis mellifera simensis)


Autoři: Haftom Gebremedhn aff001;  Bezabeh Amssalu aff003;  Lina De Smet aff001;  Dirk C. de Graaf aff001
Působiště autorů: Laboratory of Molecular Entomology and Bee Pathology, Ghent University, Ghent, Belgium aff001;  Tigray Agricultural Research Institute, Mekelle, Ethiopia aff002;  Holeta Bee Research Center, Holeta, Ethiopia aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223236

Souhrn

Worldwide, the ecto-parasitic mite Varroa destructor has been assigned as an important driver of honey bee (Apis mellifera) colony losses. Unlike the subspecies of European origin, the honey bees in some African countries such as Uganda and Ethiopia may not be as threatened or suffer less from mite-infestations. However, only little is known about the factors or traits that enable them to co-exist with the mite without beekeepers’ intervention. Hence, this study was designed to investigate these factors or traits that limit the Varroa mite population in Ethiopian honey bees (Apis mellifera simensis). The study was conducted in the primary honey producing region of Ethiopia, i.e. Tigray. Mite infestation levels were shown to be lower in traditional hives (when compared to framed hives) and when colonies were started up from swarm catching (when compared to colony splitting). However, the influence of the comb cell size on mite infestation was not observed. With respect to the bee biology, the hygienic behavior was shown to be high (pin-test: 92.2% removal in 24 hours) and was negatively correlated with phoretic mite counts (Pearson; r = -0.79; P < 0.01) and mite infestation levels in brood (Pearson; r = -0.46; P < 0.001). Efforts to estimate the Varroa mite reproductive capacity were seriously hampered by an extremely low brood infestation level. From the 133 founder mites found (in 6727 capped brood cells) only 18.80% were capable of producing a reproductive progeny. Failure to produce adult male progeny was unexpectedly high (79.70%). We have suggested a few adaptations to the test protocols allowing to estimate the protective traits of honey bee colonies under very low Varroa pressure. Apart from that, this study demonstrates that the honey bees from Ethiopia are suitable targets to further decipher the genetic predisposition of resistance against V. destructor. It is still unclear to what extent simensis differs from the more common scutellata subspecies.

Klíčová slova:

Bees – Ethiopia – Europe – Honey bees – Mites – Social systems – Beeswax – Pupae


Zdroje

1. Gallai N, Salles J-M, Settele J, Vaissière BE. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics. 2009;68(3):810–21. doi: 10.1016/j.ecolecon.2008.06.014

2. Archer CR, Pirk CWW, Carvalheiro LG, Nicolson SW. Economic and ecological implications of geographic bias in pollinator ecology in the light of pollinator declines. Oikos. 2014;123(4):401–7. doi: 10.1111/j.1600-0706.2013.00949.x

3. Chemurot M. The distribution, infestation levels and effects of honeybee parasites and pathogens on colony performance in two agro-ecological zones of Uganda. Ghent: Ghent University; 2017.

4. Muli E, Patch H, Frazier M, Frazier J, Torto B, Baumgarten T, et al. Evaluation of the distribution and impacts of parasites, pathogens, and pesticides on honey bee (Apis mellifera) populations in east Africa. Plos One. 2014;9(4):1–11. doi: 10.1371/journal.pone.0094459 24740399

5. Tantillo G, Bottaro M, Di Pinto A, Martella V, Di Pinto P, Terio V. Virus infections of honeybees Apis mellifera. Italian Journal of Food Safety. 2015;4(5364):157–68. doi: 10.4081/ijfs.2015.5364 27800411

6. VanEngelsdorp D, Jr JH, Underwood RM, Pettis J. A survey of honey bee colony losses in the U.S., fall 2007 to spring 2008. Plos One. 2008;3(12):8–13. doi: 10.1371/journal.pone.0004071 19115015

7. VanEngelsdorp D, Caron D, Hayes J, Underwood R, Rennich K, Spleen A, et al. A national survey of managed honey bee 2010–11 winter colony losses in the USA: results from the Bee Informed Partnership. J Apicult Res. 2012;51(1):115–24. doi: 10.3896/IBRA.1.51.1.14

8. Smith KM, Loh EH, Rostal MK, Zambrana-Torrelio CM, Mendiola L, Daszak P. Pathogens, pests, and economics: Drivers of honey bee colony declines and losses. EcoHealth. 2013;10(4):434–45. doi: 10.1007/s10393-013-0870-2 24496582

9. 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.

10. Higes M, Martín-hernández R, Martínez-salvador A, Garrido-bailón E, González-porto AV, Meana A, et al. A preliminary study of the epidemiological factors related to honey bee colony loss in Spain. Environmental Microbiology Reports. 2010;2(2):243–50. doi: 10.1111/j.1758-2229.2009.00099.x 23766075

11. Henry M, Béguin M, Requier F, Rollin O, Odoux J-F, Aupinel P, et al. A common pesticide decreases foraging success and survival in honey bees. Science. 2012;336(6079):348–50. doi: 10.1126/science.1215039 22461498

12. Naug D. Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biological Conservation. 2009;142(10):2369–72. doi: 10.1016/j.biocon.2009.04.007

13. Le Conte Y, Ellis M, Ritter W. Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie. 2010;41(3):353–63. doi: 10.1051/apido/2010017

14. Buchler R, Bergg S, Conte YL. Breeding for resistance to Varroa destructor in Europe. Apidologie. 2010;41:393–408. doi: 10.1051/apido/2010011

15. Rinkevich FD, Danka RG, Healy KB. Influence of varroa mite (Varroa destructor) management practices on insecticide sensitivity in the honey bee (Apis mellifera). Insects. 2017;8(9):1–12. doi: 10.3390/insects8010009 28085045

16. Begna D. Occurrences and distributions of honeybee (Apis mellifera Jemenetica) varroa mite (Varroa destructor) in Tigray Region, Ethiopia. Journal of Fisheries and Livestock Production. 2014;2(3). doi: 10.4172/2332-2608.1000126

17. Chemurot M, Akol AM, Masembe C, de Smet L, Descamps T, de Graaf DC. Factors influencing the prevalence and infestation levels of Varroa destructor in honeybee colonies in two highland agro-ecological zones of Uganda. Exp Appl Acarol. 2016;68(4):497–508. doi: 10.1007/s10493-016-0013-x WOS:000373858600008. 26801158

18. Dietemann V, Pirk CWW, Crewe R. Is there a need for conservation of honeybees in Africa? Apidologie. 2009;40(3):285–95. doi: 10.1051/apido/2009013

19. Fazier M, Muli E, Conklin T, Schmehl D, Torto B, Frazier J, et al. A scientific note on Varroa destructor found in East Africa; threat or opportunity? Apidologie. 2010;41:463–5. doi: 10.1051/apido/2009073

20. Mezgabu E, Hirpa E, Begna D, Lama Y, Bayan Aa, Misganu C. Occurrence and distribution of Varroa mite and antivarroa effect of propolis in Walmara district of Oromia special zone around Finfine, Ethiopia. Journal of Veterinary Science & Technology. 2016;7(5). doi: 10.4172/2157-7579.1000370

21. Pirk CWW, Strauss U, Yusuf AA, Demares F, Human H. Honeybee health in Africa—a review. Apidologie. 2016;47:276–300. doi: 10.1007/s13592-015-0406-6

22. Akinwande KL, Badejo M, Ogbogu SS. Incidence of the Korean haplotype of Varroa destructor in southwest Nigeria. J Apicult Res. 2012;51(4):369–70. doi: 10.3896/IBRA.1.51.4.15

23. Begna D, Gela A, Negera T, Bezabeh A. Identifying the species, effects and seasonal dynamics of honeybee varroa mites: A newly emerging parasite to Ethiopian honeybee. International Journal of Scientific Research in Environmental Science and Toxicology. 2016;1(1):4–.

24. Mumoki FN, Fombong A, Muli E, Muigai WT, Masiga D. An inventory of documented diseases of African honeybees. Afr Entomol. 2014;22(3):473–87. doi: 10.4001/003.022.0313 WOS:000344616900002.

25. Strauss U, Human H, Gauthier L, Crewe RM, Dietemann V, Pirk CWW. Seasonal prevalence of pathogens and parasites in the savannah honeybee (Apis mellifera scutellata). J Invertebr Pathol. 2013;114(1):45–52. doi: 10.1016/j.jip.2013.05.003 WOS:000322849600008. 23702244

26. Allsopp MH. Analysis of Varroa destructor infestation of Southern African honeybee populations 2006.

27. Nganso BT, Fombong AT, Yusuf AA, Pirk CWW, Stuhl C, Torto B. Hygienic and grooming behaviors in African and European honeybees—New damage categories in Varroa destructor. Plos One. 2017;12(6):1–14.

28. Strauss U, Dietemann V, Human H, Crewe RM, Pirk CWW. Resistance rather than tolerance explains survival of savannah honeybees (Apis mellifera scutellata) to infestation by the parasitic mite Varroa destructor. Parasitology. 2016;143:374–87. doi: 10.1017/S0031182015001754 26690678

29. Nganso BT, Fombong AT, Yusuf AA, Pirk CWW, Stuhl C, Torto B. Low fertility, fecundity and numbers of mated female offspring explain the lower reproductive success of the parasitic mite Varroa destructor in African honeybees. Parasitology. 2018:1–7. doi: 10.1017/S0031182018000616 29661259

30. Martin SJ, Kryger P. Reproduction of Varroa destructor in South African honey bees: does cell space influence Varroa male survivorship? Apidologie. 2002;33:51–61. doi: 10.1051/apido: 2001007.

31. Saucy F. On the natural cell size of European honey bees: a “fatal error” or distortion of historical data? J Apicult Res. 2014;53(3):327–36. doi: 10.3896/IBRA.1.53.3.01

32. Erickson EH, Lusby DA, Hoffman GD, Lusby EW. On the size of cells: speculations on foundation as a colony management tool. 1990. p. 98–101.

33. Moritz RFA. Heritability of the postcapping stage in Apis mellifera and its relation to varroatosis resistance. The Journal of Heredity. 1985;76(4):267–70.

34. Fries I, Imdorf A, Rosenkranz P. Survival of mite infested (Varroa destructor) honey bee (Apis mellifera) colonies in a Nordic climate. Apidologie. 2006;37:564–70. doi: 10.1051/apido:2006031

35. Kurze C, Routtu J, Moritz RFA. Parasite resistance and tolerance in honeybees at the individual and social level. Zoology. 2016;119(4):290–7. doi: 10.1016/j.zool.2016.03.007 27106014

36. Guerra JJCV Jr, Gonçalves LS, Jong DD. Africanized honey bees (Apis mellifera L.) are more efficient at removing worker brood artificially infested with the parasitic mite Varroa jacobsoni Oudemans than are Italian bees or Italian/Africanized hybrids. Genetics and Molecular Biology. 2000;23(1):89–92. doi: 10.1590/S1415-47572000000100016

37. Strauss U, Pirk CWW, Crewe RM, Human H, Dietemann V. Impact of Varroa destructor on honeybee (Apis mellifera scutellata) colony development in South Africa. Exp Appl Acarol. 2015;65(1):89–106. doi: 10.1007/s10493-014-9842-7 25037745

38. Arechavaleta-Velasco ME, Guzman-Novoa E. Relative effect of four characteristics that restrain the population growth of the mite Varroa destructor in honey bee (Apis mellifera) colonies. Apidologie. 2001;32:157–74. doi: 10.1051/apido:2001121

39. Oddie MAY, Dahle B, Neumann P. Norwegian honey bees surviving Varroa destructor mite infestations by means of natural selection. PeerJ. 2017;5(e3956):1–12. doi: 10.7717/peerj.3956 29085753

40. Locke B, Conte YL, Crauser D, Fries I. Host adaptations reduce the reproductive success of Varroa destructor in two distinct European honey bee populations. Ecol Evol. 2012;2(6):1144–50. doi: 10.1002/ece3.248 22833790

41. Broeckx BJG, De Smet L, Blacquière T, Kevin M, Khalenkow M, Van Poucke M, et al. Honey bee predisposition of resistance to ubiquitous mite infestations. Sci Rep-Uk. 2019;9:7794. doi: 10.1038/s41598-019-44254-8 31127129

42. Factbook CIAW. The World Factbook—Central Intelligence Agency. 2012.

43. Dong Y, Frimpong K, Haile R, Liu M, Schaffer AM, da Costa LV. Final Report for WEEMA International. 2016.

44. Unicef. Ethiopia Country Profile—unicef. 2016.

45. Mohammed NA. Geographical races of the Honeybees (Apis mellifera) of the Northern Regions of Ethiopia 2002.

46. Csa. Report on livestock and livestock characteristics (private peasant holdings). Addis Ababa: 2017.

47. Meixner MD, Leta MA, Koeniger N, Fuchs S. The honey bees of Ethiopia represent a new subspecies of Apis mellifera—Apis mellifera simensis n. ssp. Apidologie. 2011;42:425–37. doi: 10.1007/s13592-011-0007-y

48. Godifey G. Epidemiology of honey bee disease and pests in selected zones of Tigray region, Northern Ethiopia 2015.

49. Khalenkow M. Test protocols. 2018.

50. Dietemann V, Nazzi F, Martin SJ, Anderson DL, Locke B, Delaplane KS, et al. Standard methods for varroa research. J Apicult Res. 2013;52(1):1–54. doi: 10.3896/IBRA.1.52.1.09

51. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nature Methods. 2012;9(7):671–5. doi: 10.1038/nmeth.2089 22930834

52. Judd TM, Teal PEA, Hernandez EJ, Choudhury T, Hunt JH. Quantitative Differences in Nourishment Affect Caste-Related Physiology and Development in the Paper Wasp Polistes metricus. Plos One. 2015;10(2):1–18. doi: 10.1371/journal.pone.0116199 25706417

53. Spivak M, Downey LA. Field Assays for Hygienic Behavior in Honey Bees (Hymenoptera: Apidae). J Econ Entomol. 1998;91(1):64–70. doi: 10.1093/jee/91.1.64

54. Kamel SM, Strange JP, Sheppard WS. A scientific note on hygienic behavior in Apis mellifera lamarckii and A. m. carnica in Egypt. Apidologie. 2003;34(6):189–90. doi: 10.1051/apido:2003014

55. Corrêa-Marques MH, Issa MRC, De Jong D. Classification and quantification of damaged Varroa jacobsoni found in the debris of honey bee colonies as criteria for selection? Am Bee J. 2000;140(10):820–4.

56. Calderón RA, Zamora LG, Van Veen JW, Quesada aV. A comparison of the reproductive ability of Varroa destructor (Mesostigmata:Varroidae) in worker and drone brood of Africanized honey bees (Apis mellifera). Exp Appl Acarol. 2007;43(1):25–32. doi: 10.1007/s10493-007-9102-1 17828439

57. Rosenkranz P, Aumeier P, Ziegelmann B. Biology and control of Varroa destructor. J Invertebr Pathol. 2010;103:S96–S119. doi: 10.1016/j.jip.2009.07.016 19909970

58. Kebede A. Honey bee production practices and honey quality in Silti Wereda, Ethiopia 2011.

59. Piccirillo GA, Jong DD. Old honey bee brood combs are more infested by the mite Varroa destructor than are new brood combs. Apidologie. 2004;35(6):359–64. doi: 10.1051/apido:2004022

60. Pereira RA, Morais MM, Francoy TM, Gonçalves LS. Hygienic behavior of africanized honey bees Apis mellifera directed towards brood in old and new combs during diurnal and nocturnal periods. Insects. 2013;4:521–32. doi: 10.3390/insects4040521 26462521

61. Coffey MF, Breen J, Brown MJF, McMullan JB. Brood-cell size has no influence on the population dynamics of Varroa destructor mites in the native western honey bee, Apis mellifera mellifera. Apidologie. 2010;41:522–30. doi: 10.1051/apido/2010003

62. Taylor MA, Goodwin RM, McBrydie HM, Cox HM. The effect of honey bee worker brood cell size on Varroa destructor infestation and reproduction. Journal of Apicultural Research and Bee World. 2008;47(4):239–42. doi: 10.3896/IBRA.1.47.4.01

63. Piccirillo GA, De Jong D. The influence of brood comb cell size on the reproductive behavior of the ectoparasitic mite Varroa destructor in Africanized honey bee colonies. Genetics and Molecular Research. 2003;2(1):36–42. 12917800

64. Ardestani MM. Investigating the influence of postcapping period on varroa mite infestation. J Apicult Res. 2016;54(4):334–40. doi: 10.1080/00218839.2016.1159788

65. Abejew TA, Zeleke ZM. Study on the beekeeping situation, the level of beekeepers bnowledge concerning local honeybee subspecies, their productive characteristics, and behavior in eastern Amhara region, Ethiopia. Advances in Agriculture. 2017;2017:1–7. doi: 10.1155/2017/6354250

66. Hepbum HR, Radloff SE. Honeybees of Africa. 1st editi ed. New York: Springer-Verlag Berlin Heidelberg; 1998. 377- p.

67. Nuru A, Amssalu B, Hepburn HR, Radloff SE. Swarming and migration in the honey bees (Apis mellifera) of Ethiopia. J Apicult Res. 2002;41(1–2):35–41. doi: 10.1080/00218839.2002.11101066

68. Gebremedhn H, Tesfay Z, Murutse G, Estifanos A. Seasonal honeybee forage availability, swarming, absconding and honey harvesting in Debrekidan and Begasheka watersheds of Tigray, Northern Ethiopia. 2013.

69. Abazinab M, Debele K, Worku Z. Assessment of beekeeping practices in Shabe and Seka Chekorsa districts of Jimma zone, Southwestern Ethiopia. European Journal of Biological Science. 2016;8(2):45–55. doi: 10.5829/idosi.ejbs.2016.8.02.23966

70. Gebretsadik T, Negash D. Honeybee production system, challenges and opportunities in selected districts of Gedeo zone, Southern Nation, Nationalities and Peoples Regional State, Ethiopia. International Journal of Research Granthaalayah. 2016;4(4).

71. Tilahun M, Abraha Z, Gebre A, Drumond P. Beekeepers’ honeybee colony selection practice in Tigray, Northern Ethiopia. Livestock Research for Rural Development. 2016;28(5).

72. Arathi HS, Burns I, Spivak M. Ethology of hygienic behaviour in the honey bee Apis mellifera L-(Hymenoptera: Apidae): Behavioural repertoire of hygienic bees. Ethology. 2000;106(4):365–79. doi: 10.1046/j.1439-0310.2000.00556.x WOS:000086783400006.

73. Spivak M, Reuter GS. Performance of hygienic honey bee colonies in a commercial apiary. Apidologie. 1998;29(3):291–302. doi: 10.1051/apido:19980308 WOS:000073978100008.

74. Boecking O, Drescher W. The Removal Response of Apis-Mellifera L Colonies to Brood in Wax and Plastic Cells after Artificial and Natural Infestation with Varroa-Jacobsoni Oud and to Freeze-Killed Brood. Experimental & Applied Acarology. 1992;16(4):321–9. doi: 10.1007/Bf01218574 WOS:A1992KM78900007.

75. Spivak M. Honey bee hygienic behavior and defense against Varroa jacobsoni. Apidologie. 1996;27(4):245–60. doi: 10.1051/apido:19960407 WOS:A1996VY68300007.

76. Stanimirovic Z, Pejovic D, Stevanovic J, Vucinic M, Mirilovic M. Investigations of hygienic behaviour and disease resistance in organic beekeeping of two honeybee ecogeographic varieties from Serbia. Acta Vet-Beograd. 2002;52(2–3):169–79. doi: 10.2298/Avb0203169s WOS:000176114300012.

77. Guzman LID, Rinderer TE, Stelzer JA, Beaman L, Delatte GT, Harper C. Hygienic behavior by honey bees from far-eastern Russia. Am Bee J. 2002;142:58–60.

78. Spivak M, Downey DL. Field assays for hygienic behavior in honey bees (Hymenoptera: Apidae). J Econ Entomol. 1998;91(1):64–70. doi: 10.1093/jee/91.1.64 WOS:000073139800009.

79. Alemu T, Legesse G, Ararso Z. Performance evaluation of honeybee (Apis mellifera scutellata) in Guji Zone. International Journal of Innovation and Applied Studies. 2014;9(4):1987–93.

80. Corrêa-Marques MH, Medina LM, Martin SJ, De Jong D. Comparing data on the reproduction of Varroa destructor. Genetics and Molecular Research. 2003;2(1):1–6. 12917797

81. Caldero RA, Uren S, Veen JWV. Reproduction of Varroa destructor and offspring mortality in worker and drone brood cells of Africanized honey bees. Exp Appl Acarol. 2012;56:297–307. doi: 10.1007/s10493-012-9518-0 22270116

82. Cameron SJ. Colour changes in honeybee pupae. Bee World. 1962;43(4):119–22. doi: 10.1080/0005772X.1962.11096960

83. Panziera D, Langevelde F, Blacquiere T. Varroa sensitive hygiene contributes to naturally selected varroa resistance in honey bees. J Apicult Res. 2017;56(5):635–42. doi: 10.1080/00218839.2017.1351860 WOS:000413469200017.

84. Garrido C, Rosenkranz P. Volatiles of the honey bee larva initiate oogenesis in the parasitic mite Varroa destructor. Chemoecology. 2004;14(3–4):193–7. doi: 10.1007/s00049-004-0278-0 WOS:000224526000008.


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