Advertisement

Dominant honeybee colony infestation by Varroa destructor (Acari: Varroidae) K haplotype in Japan

  • 8 Accesses

Abstract

Varroa destructor Anderson and Trueman (Acari: Varroidae) are ectoparasitic mites found in the western honeybee Apis mellifera Linnaeus (Hymenoptera: Apidae). Varroa destructor is classified into two haplotypes, i.e., Korea (K) and Japan (J), based on mtDNA sequences. Among these, V. destructor K haplotype is possibly a more severe threat to A. mellifera colonies. Previous studies collected both V. destructor haplotypes from honeybee colonies in Japan. However, no detailed surveillance of infestation of Japanese apiaries by V. destructor or identification of their genetic structure has been conducted to date. We surveyed V. destructor at 15 different Japanese apiaries of A. mellifera. Varroa destructor was collected from 14 Japanese apiaries, and all mites were classified as V. destructor K haplotype. Varroa destructor infestation of the Japanese honeybee A. cerana japonica Radoszkawsi (Hymenoptera: Apidae) was also analyzed. Varroa destructor K haplotype was predominant in A. cerana colonies. Despite the different host species, all collected V. destructor K haplotype samples were classified into a single haplogroup, i.e., K1-1/K1-2. These results indicate that A. mellifera and A. cerana were infested by the same V. destructor haplogroup. This is the first report detailing a survey on V. destructor prevalence and haplogroups among Japanese apiaries.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3

References

  1. Anderson DL, Fuchs S (1998) Two genetically distinct populations of Varroa jacobsoni with contrasting reproductive abilities on Apis mellifera. J Apic Res 37:69–78. https://doi.org/10.1080/00218839.1998.11100957

  2. Anderson DL, Trueman JW (2000) Varroa jacobsoni (Acari: Varroidae) is more than one species. Exp Appl Acarol 24:165–189

  3. Beaurepaire AL, Truong TA, Fajardo AC et al (2015) Host specificity in the honeybee parasitic mite, Varroa spp in Apis mellifera and Apis cerana. PLoS ONE 10:e0135103. https://doi.org/10.1371/journal.pone.0135103

  4. Boecking O, Genersch E (2008) Varroosis—the ongoing crisis in bee keeping. J Verbrauch Lebensm 3:221–228. https://doi.org/10.1007/s00003-008-0331-y

  5. Boot WJ, Tan NQ, Dien PC et al (1997) Reproductive success of Varroa jacobsoni in brood of its original host, Apis cerana, in comparison to that of its new host, A. mellifera (Hymenoptera: Apidae). B Entomol Res 87:119–126. https://doi.org/10.1017/S0007485300027255

  6. Branco MR, Kidd NAC, Pickard RS (1999) Development of Varroa jacobsoni in colonies of Apis mellifera iberica in a Mediterranean climate. Apidologie 30:491–503

  7. Crane E (1978) The Varroa mite. Bee World 59:164. https://doi.org/10.1080/0005772X.1978.11097718

  8. Currie RW, Gatien P (2006) Timing acaricide treatments to prevent Varroa destructor (Acari: Varroidae) from causing economic damage to honey bee colonies. Can Entomol 138:238–252

  9. Dainat B, Evans JD, Chen YP et al (2012) Dead or alive: deformed wing virus and Varroa destructor reduce the life span of winter honeybees. Appl Environ Microbiol 78:981–987. https://doi.org/10.1128/AEM.06537-11

  10. de Guzman LI, Rinderer TE, Stelzer JA (1997) DNA evidence of the origin of Varroa jacobsoni Oudemans in the Americas. Biochem Genet 35:327–335. https://doi.org/10.1023/A:1021821821728

  11. de Guzman LI, Rinderer TE, Stelzer JA (1999) Occurrence of two genotypes of Varroa in North America. Apidologie 30:31–36

  12. De Jong D, De Jong PH, Gonçalves LS (1982) Weight loss and other damage to developing worker honeybees from infestation with V. jacobsoni. J Apic Res 21:165–216. https://doi.org/10.1080/00218839.1982.11100535

  13. Dietemann V, Nazzi F, Martin SJ et al (2015) Standard methods for Varroa research. J Apic Res 52:1–54. https://doi.org/10.3896/IBRA.1.52.1.09

  14. Delfinado-Baker (1988) Variability and biotypes of Varroa jacobsoni Oudemans. Am Bee J 128:567–568

  15. Duay P, De Jong D, Engels W (2002) Decreased flight performance and sperm production in drones of the honeybee (Apis mellifera) slightly infested by Varroa destructor mites during pupal development. Genet Mol Res 1:227–232

  16. Duay P, De Jong D, Engels W (2003) Weight loss in drone pupae (Apis mellifera) multiply infested by Varroa destructor mites. Apidologie 34:61–65. https://doi.org/10.1051/apido:2002052

  17. Dynes TL, De Roode JC, Lyons JI et al (2016) Fine scale population genetic structure of Varroa destructor, an ectoparasitic mite of the honey bee (Apis mellifera). Apidologie 48:93–101. https://doi.org/10.1007/s13592-016-0453-7

  18. Evans JD, Cook SC (2018) Genetics and physiology of Varroa mites. Curr Opin Insect Sci 26:130–135. https://doi.org/10.1016/j.cois.2018.02.005

  19. Evans JD, Lopez DL (2002) Complete mitochondrial DNA sequence of the important honey bee pest, Varroa destructor (Acari: Varroidae). Exp Appl Acarol 27:69–78

  20. Farjamfar M, Saboori A, Gonzalez-Cabrera J, Hernandez Rodriguez CS (2018) Genetic variability and pyrethroid susceptibility of the parasitic honey bee mite Varroa destructor (Acari: Varroidae) in Iran. Exp Appl Acarol 76:139–148. https://doi.org/10.1007/s10493-018-0296-1

  21. Forfert N, Natsopoulou ME, Frey E et al (2015) Parasites and pathogens of the honeybee (Apis mellifera) and their influence on inter-colonial transmission. PLoS ONE 10:1–14. https://doi.org/10.1371/journal.pone.0140337

  22. Fries I, Huazhen W, Wei S, Jin CS (1996) Grooming behavior and damaged mites (Varroa jacobsoni) in Apis cerana cerana and Apis mellifera ligustica. Apidologie 27:3–11. https://doi.org/10.1051/apido:19960101

  23. Gajić B, Radulović Ž, Stevanović J et al (2013) Variability of the honey bee mite Varroa destructor in Serbia, based on mtDNA analysis. Exp Appl Acarol 61:97–105. https://doi.org/10.1007/s10493-013-9683-9

  24. Gajić B, Stevanović J, Radulović Ž et al (2016) Haplotype identification and detection of mitochondrial DNA heteroplasmy in Varroa destructor mites using ARMS and PCR–RFLP methods. Exp Appl Acarol 70:287–297. https://doi.org/10.1007/s10493-016-0086-6

  25. Garedew A, Schmolz E, Lamprecht I (2004) The energy and nutritional demand of the parasitic life of the mite Varroa destructor. Apidologie 35:419–430. https://doi.org/10.1051/apido:2004032

  26. Garrido C, Rosenkranz P, Paxton RJ, Gonçalves LS (2003) Temporal changes in Varroa destructor fertility and haplotype in Brazil. Apidologie 34:535–541. https://doi.org/10.1051/apido:2003041

  27. Gatien P, Currie R (2003) Timing of acaricide treatments for control of low-level populations of Varroa destructor (Acari: Varroidae) and implications for colony performance of honey bees. Can Entomol 135:749–763. https://doi.org/10.4039/n02-086

  28. Guerra JJ, Issa M, Carneiro F et al (2010) RAPD identification of Varroa destructor genotypes in Brazil and other regions of the Americas. Genet Mol Res 9:303–308. https://doi.org/10.4238/vol9-1gmr696

  29. Guzmán-Novoa E, Eccles L, Calvete Y et al (2010) Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie 41:443–450. https://doi.org/10.1051/apido/2009076

  30. Hedtke K, Jensen PM, Jensen AB, Genersch E (2011) Evidence for emerging parasites and pathogens influencing outbreaks of stress-related diseases like chalkbrood. J Invertebr Pathol 108:167–173. https://doi.org/10.1016/j.jip.2011.08.006

  31. Kelomey AE, Paraiso A, Sina H et al (2017) Genetic characterization of the honeybee ectoparasitic mite Varroa destructor from Benin (West Africa) using mitochondrial and microsatellite markers. Exp Appl Acarol 72:61–67. https://doi.org/10.1007/s10493-017-0141-y

  32. Kralj J, Fuchs S (2006) Parasitic Varroa destructor mites influence flight duration and homing ability of infested Apis mellifera foragers. Apidologie 37:577–587. https://doi.org/10.1051/apido:2006040

  33. Kralj J, Brockmann A, Fuchs S, Tautz J (2007) The parasitic mite Varroa destructor affects non-associative learning in honey bee foragers, Apis mellifera L. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193:363–370. https://doi.org/10.1007/s00359-006-0192-8

  34. Kraus B, Hunt G (1995) Differentiation of Varroa jacobsoni Oud populations by random amplification of polymorphic DNA (RAPD). Apidologie 26:283–290. https://doi.org/10.1051/apido:19950402

  35. Livestock Farming Promotion Division, Bureau for Promotion of Agricultural Production of Hokkaido Pref. (2018) Status of beekeeping in Hokkaido Prefecture (Hokkaido no youhou wo meguru jyousei, in Japanese (https://www.pref.hokkaido.lg.jp/ns/tss/35/hachi/youhouwomegurujyousei.pdf)

  36. MAFF (Ministry of Agriculture, Forestry and Fisheries) (2018) Annual report of monitored infectious diseases at act on domestic animal infectious diseases control (Kanshi densenbyou hassei nenpyou, in Japanese) (https://www.maff.go.jp/j/syouan/douei/kansi_densen/attach/pdf/kansi_densen-146.pdf)

  37. Maggi M, Medici S, Quintana S et al (2012) Genetic structure of Varroa destructor populations infesting Apis mellifera colonies in Argentina. Exp Appl Acarol 56:309–318. https://doi.org/10.1007/s10493-012-9526-0

  38. Martin SJ (2001) The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach. J Appl Ecol 38:1082–1093. https://doi.org/10.2307/827245

  39. Muñoz I, Garrido-Bailón E, Martín-Hernández R et al (2008) Genetic profile of Varroa destructor infesting Apis mellifera iberiensis colonies. J Apic Res 47:310–313. https://doi.org/10.1080/00218839.2008.11101480

  40. Navajas M, Anderson DL, de Guzman LI et al (2010) New Asian types of Varroa destructor : a potential new threat for world apiculture. Apidologie 41:181–193. https://doi.org/10.1051/apido/2009068

  41. Navajas M, Le Conte Y, Solignac M et al (2002) The complete sequence of the mitochondrial genome of the honeybee ectoparasite mite Varroa destructor (Acari: Mesostigmata). Mol Biol Evol 20:2313–2317. https://doi.org/10.1093/oxfordjournals.molbev.a004055

  42. Nazzi F, Brown SP, Annoscia D et al (2012) Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honeybee colonies. Plos Pathog 8:e1002735. https://doi.org/10.1371/journal.ppat.1002735

  43. Ogihara MH, Stoich M, Morimoto N, Yoshiyama M, Kimura K (2020) Roasted soybean flour as an alternative powder roll substrate for Varroa mite detection

  44. R Development Core Team (2013) R: A Language and environment for statistical computing. R foundation for statistical computing, Vienna

  45. Ramsey SD, Ochoa R, Bauchan G et al (2019) Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proc Natl Acad Sci USA 116:1792–1801. https://doi.org/10.1073/pnas.1818371116

  46. Ratti V, Kevan PG, Eberl HJ (2015) A mathematical model of the honeybee-Varroa destructor-acute bee paralysis virus system with seasonal effects. B Math Biol 77:1493–1520. https://doi.org/10.1007/s11538-015-0093-5

  47. Roberts JMK, Anderson DL, Tay WT (2015) Multiple host shifts by the emerging honeybee parasite, Varroa jacobsoni. Mol Ecol 24:2379–2391. https://doi.org/10.1111/mec.13185

  48. Sakai T, Okada I (1973) The present beekeeping in Japan. Glean Bee Cult 101:356–357

  49. Schneider P, Drescher W (1987) The influence of Varroa jacobsoni Oud. on weight, development of weight and hypopharyngeal glands, and longevity of Apis mellifera L. Apidologie 18:101–110

  50. Shimanuki H, Calderone NW, Knox DA (1994) Parasitic mite syndrome: the symptoms. Am Bee J 134:827–828

  51. Solignac M, Cornuet J-M, Vautrin D et al (2005) The invasive Korea and Japan types of Varroa destructor, ectoparasitic mites of the Western honeybee (Apis mellifera), are two partly isolated clones. Proc Biol Sci 272:411–419. https://doi.org/10.1098/rspb.2004.2853

  52. Solignac M, Vautrin D, Pizzo A et al (2003) Characterization of microsatellite markers for the apicultural pest Varroa destructor (Acari: Varroidae) and its relatives. Mol Ecol Notes 3:556–559. https://doi.org/10.1046/j.1471-8286.2003.00510.x

  53. Strapazzon R, Carneiro FE, Guerra JCVJ, Moretto G (2009) Genetic characterization of the mite Varroa destructor (Acari: Varroidae) collected from honey bees Apis mellifera (Hymenoptera, Apidae) in the state of Santa Catarina, Brazil. Genet Mol Res 8:990–997. https://doi.org/10.4238/vol8-3gmr567

  54. Strange JP, Sheppard WS (2001) Optimum timing of miticide applications for control of Varroa destructor (Acari: Varroidae) in Apis mellifera (Hymenoptera: Apidae) in Washington State, USA. J Econ Entomol 94:1324–1331. https://doi.org/10.1603/0022-0493-94.6.1324

  55. Techer MA, Rane RV, Grau ML et al (2019) Divergent evolutionary trajectories following speciation in two ectoparasitic honey bee mites. Commun biol 2:357. https://doi.org/10.1038/s42003-019-0606-0

  56. van Dooremalen C, Gerritsen L, Cornelissen B et al (2012) Winter survival of individual honey bees and honey bee colonies depends on level of Varroa destructor infestation. PLoS ONE 7:e36285. https://doi.org/10.1371/journal.pone.0036285

  57. Warrit N, Smith DR, Lekprayoon C (2006) Genetic subpopulations of Varroa mites and their Apis cerana hosts in Thailand. Apidologie 37:19–30. https://doi.org/10.1051/apido:2005051

  58. Warrit N, Hagen TAR, Smith DR, Çakmak I (2015) A survey of Varroa destructor strains on Apis mellifera in Turkey. J Apic Res 43:190–191. https://doi.org/10.1080/00218839.2004.11101137

  59. Yoshiyama M, Kimra K (2018) Bee diversity and current status of beekeeping in Japan. In: Chantawannakul P, Williams G, Neumann P (eds) Asian beekeeping in the twenty-first century. Springer, Berlin, pp 223–246

  60. Zhou T, Anderson DL, Huang ZY et al (2004) Identification of Varroa mites (Acari: Varroidae) infesting Apis cerana and Apis mellifera in China. Apidologie 35:645–654. https://doi.org/10.1051/apido:2004059

Download references

Acknowledgements

We would like to express our gratitude to all beekeepers for allowing our surveillance and V. destructor collection. We are grateful to Dr. Taro Maeda (Institute of Agrobiological Sciences, National Agriculture and Food Research Organization) for providing V. destructor collected from A. cerana colonies. We want to thank Ms. Noriko Takano, Ms. Mai Wakasa, and Mr. Mitsugu Ebihara for surveillance preparation. The authors would like to thank Enago (www.enago.jp) for the English language review.

Author information

Correspondence to Mari H. Ogihara.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ogihara, M.H., Yoshiyama, M., Morimoto, N. et al. Dominant honeybee colony infestation by Varroa destructor (Acari: Varroidae) K haplotype in Japan. Appl Entomol Zool (2020) doi:10.1007/s13355-020-00667-w

Download citation

Keywords

  • Varroa destructor
  • Apis mellifera
  • Apis cerana
  • Haplotype
  • Beekeeping