Advertisement

The Overview of Honey Bee Diversity and Health Status in Asia

  • Panuwan Chantawannakul
  • Samuel Ramsey
Chapter

Abstract

 Traditional honey bee hunting and beekeeping are vital to the economic and spiritual lives of Asians. Bee products are known as not only food/food supplement but also traditional medicine for aiming to promote good health, especially in eastern regions. Honey bees also play crucial roles in pollination. Asia is regarded as the homeland of honey bees as it hosts at least nine honey bee species. The European honey bee was introduced from Europe, North America, and Oceania to Russia, Japan, India and other countries in Asia. The growth of global human population size, globalized trade economic wealth, and technological developments in transportation efficacy has promoted the transmission of bee diseases, parasites and pests. A great concern over honeybee population decline has accelerated research in bee diseases, parasites, and pests. This chapter provides an up-to-date information on bee diseases, parasites, and pests in Asia.

Keywords

Asian honey bee Thai bee Apis dorsata Thai honey Apis cerana 

Notes

Acknowledgement

PC would like to acknowledge Thailand research fund ((RSA6080028) and Chiang Mai University fund. SR would like to acknowledge funding provided by the vanEngelsdorp lab at the University of Maryland and the encouragement/support of Dr. Dennis vanEngelsdorp.

References

  1. Abrol DP, Bhat AA (1990) Studies on ‘Thai sac brood virus’ affecting indigenous honeybee Apis cerana indica Fab. colonies - prospects and future strategies – I. J Anim Morphol Physiol 37:101–108Google Scholar
  2. Abrol DP, Putatunda BN (1996) New record of Tropilaelaps clareae (Acarina: Mesostigmata) associated with Xylocopa irridipennis from India. Sci Cult 62:59Google Scholar
  3. Ai H, Yan X, Han R (2012) Occurrence and prevalence of seven bee viruses in Apis mellifera and Apis cerana apiaries in China. J Invertebr Pathol 109(1):160–164CrossRefPubMedGoogle Scholar
  4. Akrantanakul P (1987) Honey bee diseases and enemies in Asia. In: A parasitoidal guide. FAO, RomeGoogle Scholar
  5. Allen M, Ball B (1996) The incidence and world distribution of honey bee viruses. Bee World 77:141–162.  https://doi.org/10.1080/0005772X.1996.11099306 CrossRefGoogle Scholar
  6. Amr SZ, Shehada SE, Abo-Shehada M et al (1998) Honey bee parasitic arthropods in Jordan. Apiacta 3:78–82Google Scholar
  7. Anderson DL (1984) A comparison of serological techniques for detecting and identifying honeybee viruses. J Invertebr Pathol 44:233–243.  https://doi.org/10.1016/0022-2011(84)90019-3 CrossRefGoogle Scholar
  8. Anderson DL (2004) Varroa mites and their host relationships in the Philippines. In: Proceedings of the 7th Asian apicultural association conference and 10th beenet symposium and technoflora, Laguna, Luzon, Philippines, pp 177–178Google Scholar
  9. 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 CrossRefGoogle Scholar
  10. Anderson DL, Morgan MJ (2007) Genetic and morphological variation of bee-parasitic Tropilaelaps mites (Acari: Laelapidae): new and re-defined species. Exp Appl Acarol 43:1–24.  https://doi.org/10.1007/s10493-007-9103-0 CrossRefPubMedGoogle Scholar
  11. Anderson DL, Roberts JMK (2013) Standard methods for Tropilaelaps mites research. J Apic Res 52:1–16.  https://doi.org/10.3896/IBRA.1.52.4.21 CrossRefGoogle Scholar
  12. Anderson D, Giacon H, Gibson N (1997) Detection and thermal destruction of the chalkbrood fungus (Ascosphaera apis) in honey. J Apic Res 36:163–168.  https://doi.org/10.1080/00218839.1997.11100944 CrossRefGoogle Scholar
  13. Anderson DL, Sukarsih (1996) Changed Varroa jacobsoni reproduction in Apis mellifera colonies in Java. Apidologie 27:461–466CrossRefGoogle Scholar
  14. Anderson DL, Trueman JW (2000) Varroa jacobsoni (Acari: Varroidae) is more than one species. Exp Appl Acarol 24:165–189CrossRefPubMedGoogle Scholar
  15. Ansari MJ, Al-Ghamdi A, Nuru A, Ahmed AM, Ayaad TH, Al-Qarni A, Alattal Y, Al-Waili N (2017) Survey and molecular detection of Melissococcus plutonius, the causative agent of European foulbrood in honeybees in Saudi Arabia. Saudi J Biol Sci 24(6):1327–1335.  https://doi.org/10.1016/j.sjbs.2016.10.012 CrossRefPubMedGoogle Scholar
  16. Arai R, Tominaga K, Wu M et al (2012) Diversity of Melissococcus plutonius from honey bee larvae in Japan and experimental reproduction of European foulbrood with cultured atypical isolates. PLoS One 7:e33708.  https://doi.org/10.1371/journal.pone.0033708 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Arias MC, Sheppard WS (2005) Phylogenetic relationships of honey bees (Hymenoptera: Apinae: Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol Phylogenet Evol 37:25–35CrossRefPubMedGoogle Scholar
  18. Aronstein KA, Murray KD (2010) Chalkbrood disease in honey bees. J Invertebr Pathol 103(Suppl 1):S20–S29.  https://doi.org/10.1016/j.jip.2009.06.018 CrossRefPubMedGoogle Scholar
  19. Bailey L, Carpenter JM, Woods RD (1982) The diminished incidence of Acarapis woodi (Rennie) (Acari: Tarsonelidae) in honeybee, Apis mellifera L. (Hymenoptera: Apidae), in Britain. B Entomol Res 72:655–662CrossRefGoogle Scholar
  20. Beetsma J, Boot WJ, Calis J (1999) Invasion behaviour of Varroa jacobsoni Oud.: from bees into brood cells. Apidologie 30:125–140CrossRefGoogle Scholar
  21. Bharadwaj RK (1968) A new record of mite, Tropilaelaps clareae from Apis dorsata. Bee World 49:115CrossRefGoogle Scholar
  22. Boecking O, Spivak M (1999) Behavioral defenses of honey bees against Varroa jacobsoni Oud. Apidologie 30:141–158.  https://doi.org/10.1051/apido:19990205 CrossRefGoogle Scholar
  23. Booppha B, Eittsayeam S, Pengpat K et al (2010) Development of bioactive ceramics to control mite and microbial diseases in bee farms. Adv Mater Res 93:553–557CrossRefGoogle Scholar
  24. 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). Bull Entomol Res 87:119–126CrossRefGoogle Scholar
  25. Botías C, Anderson DL, Meana A et al (2012) Further evidence of an oriental origin for Nosema ceranae (Microsporidia: Nosematidae). J Invertebr Pathol 110:108–113.  https://doi.org/10.1016/j.jip.2012.02.014 CrossRefPubMedGoogle Scholar
  26. Brion ACB (2015) Small hive beetle poses threat to bee industry. Available via the Philippine star. https://www.philstar.com/business/agriculture/2015/02/22/1426217/small-hive-beetle-poses-threat-bee-industry. Accessed 22 Nov 2017
  27. Buawangpong N, de Guzman LI, Khongphinitbunjong K et al (2015) Prevalence and reproduction of Tropilaelaps mercedesae and Varroa destructor in concurrently infested Apis mellifera colonies. Apidologie 46:779–786.  https://doi.org/10.1007/s13592-015-0368-8 CrossRefGoogle Scholar
  28. Büchler R, Drescher W, Tornier I (1992) Grooming behaviour of Apis cerana, Apis mellifera and Apis dorsata and its effects on the parasitic mites Varroa jacobsoni and Tropilaelaps clareae. Exp Appl Acarol 16:313–319CrossRefGoogle Scholar
  29. Burgett DM, Kitprasert C (1990) Evaluation of Apistan as a control for Tropilaelaps clareae (Acari: Laelapidae), an Asian honey bee brood mite parasite. Am Bee J 130:51–53Google Scholar
  30. Burgett M, Akratanakul P, Morse RA (1983) Tropilaelaps clareae: a parasite of honeybees in South-East Asia. Bee World 64:25–28.  https://doi.org/10.1080/0005772X.1983.11097904 CrossRefGoogle Scholar
  31. Camphor ESW, Hashmi AA, Ritter W et al (2005) Seasonal changes in mite (Tropilaelaps clareae) and honeybee (Apis mellifera) populations in Apistan treated and untreated colonies. Apiacta 40:34–44Google Scholar
  32. Cervancia C (1993) Philippines beekeeping: status of research and development. In: Proc. Beenet Asia, pp 49–63Google Scholar
  33. Chaimanee V, Warrit N, Chantawannakul P (2010) Infections of Nosema ceranae in four different honeybee species. J Invertebr Pathol 105:207–210CrossRefPubMedGoogle Scholar
  34. Chandler D, Davidson G, Pell JK, Ball BV et al (2000) Fungal biocontrol of acari. Biocontrol Sci Technol 10:357–384.  https://doi.org/10.1080/09583150050114972 CrossRefGoogle Scholar
  35. Chantawannakul P, Dancer BN (2001) American foulbrood in honey bees. Bee World 82:168–180CrossRefGoogle Scholar
  36. Chantawannakul P, Puchanichanthranon T, Wongsiri S (2005) Inhibitory effects of some medicinal plant extracts on the growth of Ascosphaera apis. Acta Hortic 678:183–189CrossRefGoogle Scholar
  37. Chantawannakul P, Ward L, Boonham N et al (2006) A scientific note on the detection of honey bee viruses using real-time PCR (TaqMan) in Varroa mites collected from a Thai honeybee (Apis mellifera) apiary. J Invertebr Pathol 91:69–73.  https://doi.org/10.1016/j.jip.2005.11.001 CrossRefPubMedGoogle Scholar
  38. Chantawannakul P, de Guzman LI, Li J et al (2016) Parasites, pathogens, and pests of honeybees in Asia. Apidologie 47:301–324.  https://doi.org/10.1007/s13592-015-0407-5 CrossRefGoogle Scholar
  39. Chen YP, Huang ZY (2010) Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia. Apidologie 41:364–374.  https://doi.org/10.1051/apido/2010021 CrossRefGoogle Scholar
  40. Chen YP, Siede R (2007) Honey bee viruses. In: Karl Maramorosch AJS, Frederick AM (eds) Advances in virus research, vol 70. Academic, London, pp 33–80Google Scholar
  41. Chen YW, Wang C, James A et al (2000) Susceptibility of the Asian honey bee, Apis cerana, to American foulbrood, Paenibacillus larvae larvae. J Apic Res 39:169–175CrossRefGoogle Scholar
  42. Chen YP, Zhao Y, Hammond J et al (2004) Multiple virus infections in the honeybee and genome divergence of honeybee viruses. J Invertebr Pathol 87:84–93CrossRefPubMedGoogle Scholar
  43. Chen YP, Evans J, Feldlaufer M (2006a) Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. J Invertebr Pathol 92:152–159.  https://doi.org/10.1016/j.jip.2006.03.010 CrossRefPubMedGoogle Scholar
  44. Chen YP, Pettis JS, Collins A et al (2006b) Prevalence and transmission of honeybee viruses. Appl Environ Microbiol 72:606–611.  https://doi.org/10.1128/AEM.72.1.606-611.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Choe SE, Nguyen LTK, Noh JH et al (2012) Prevalence and distribution of six bee viruses in Korean Apis cerana populations. J Invertebr Pathol 109:330–333.  https://doi.org/10.1016/j.jip.2012.01.003 CrossRefPubMedGoogle Scholar
  46. Crane E (1990) Bees and beekeeping: science, practice and world resources. In: Bees and beekeeping: science, practice and world resources. pp xvii-+614Google Scholar
  47. Crane E (1999) The world history of beekeeping and honey hunting. Gerald Duckworth & Co, Ltd, LondonGoogle Scholar
  48. Dainat B, Ken T, Berthoud H et al (2009) The ectoparasitic mite Tropilaelaps mercedesae (Acari, Laelapidae) as a vector of honeybee viruses. Insect Soc 56:40–43.  https://doi.org/10.1007/s00040-008-1030-5 CrossRefGoogle Scholar
  49. Davis C, Ward W (2003) Control of chalkbrood disease with natural products: a report for the Rural Industries Research and Development Corporation. RIRDC publication no. 03/107, KingstonGoogle Scholar
  50. de Guzman LI, Delfinado-Baker M (1996) A new species of Varroa (Acari: Varroidae) associated with Apis koschevnikovi (Apidae: Hymenoptera) in Borneo. Int J Acarol 22:23–27.  https://doi.org/10.1080/01647959608684077 CrossRefGoogle Scholar
  51. de Guzman LI, Frake AM (2007) Temperature affects Aethina tumida (Coleoptera: Nitidulidae) development. J Apic Res 46:88–93.  https://doi.org/10.1080/00218839.2007.11101373 CrossRefGoogle Scholar
  52. de Guzman LI, Rinderer TE (1998) Distribution of the Japanese and Russian genotypes of Varroa jacobsoni. Honey Bee Sci 19:115–119Google Scholar
  53. de Guzman LI, Rinderer TE (1999) Identification and comparison of Varroa species infesting honey bees. Apidologie 30:85–95CrossRefGoogle Scholar
  54. de Guzman LI, Burgett M, Rinderer TE (2001) Biology and life history of Acarapis dorsalis and Acarapis externus Mites of the honey bee. Dadant, Hamilton, pp 17–27Google Scholar
  55. de Guzman LI, Rinderer TE, Frake AM (2015) The effects of diet, mating duration, female to male ratios, and temperature on ovary activation, mating success, and fecundity of Aethina tumida. Apidologie 46:326–336.  https://doi.org/10.1007/s13592-014-0325-y CrossRefGoogle Scholar
  56. de Guzman LI, Williams GR, Khongphinitbunjong K et al (2017) Ecology, life history and management of Tropilaelaps Mites. J Econ Entomol 110(2):319–332CrossRefPubMedGoogle Scholar
  57. De Jong D (1988) Varroa jacobsoni does reproduce in worker cells of Apis cerana in South Korea. Apidologie 19:241–244CrossRefGoogle Scholar
  58. de Miranda JR, Bailey L, Ball BV et al (2013) Standard methods for virus research in Apis mellifera. J Apic Res 52:1–56.  https://doi.org/10.3896/IBRA.1.52.4.22 CrossRefGoogle Scholar
  59. Decandido R, Allen D, Yosef KR et al (2004) A comparison of spring migration phenology of bee-eaters and oriental honey-buzzards Pernis ptilorhyncus at Tanjung Tuan, Malaysia, 2000-01. Ardea 92:169–174Google Scholar
  60. Delfinado MD, Baker EW (1961) Tropilaelaps, a new genus of mite from the Philippines (Laelaptidae (s. Lat.): Acarina). Chicago Nat. Hist. MuseumGoogle Scholar
  61. Delfinado MD, Baker EW (1974) Varroidae, a new family of mites on honey bees (Mesostigmata: Acarina). J Wash Acad Sci 64:4–10Google Scholar
  62. Delfinado-Baker M, Aggarwal K (1987) A new Varroa (Acari: Varroidae) from the nest of Apis cerana (Apidae). Int J Acarol 13:233–237CrossRefGoogle Scholar
  63. Delfinado-Baker M, Baker EW (1982) A new species of Tropilaelaps parasitic on honey bees. Am Bee J 122:416–417Google Scholar
  64. Delfinado-Baker M, Baker EW, Phoon ACG (1989) Mites (Acari) associated with bees (Apidae) in Asia, with description of a new species. Am Bee J 129:609–613Google Scholar
  65. Eckert JE (1961) Acarapis mites of the honey bee Apis mellifera L. J Insect Pathol 3:409–425Google Scholar
  66. Eickwort GC (1990) Biogeography and taxonomy of honey bees. Am Entomol 36:58–59CrossRefGoogle Scholar
  67. Flores JM, Spivak M, Gutiérrez I (2005) Spores of Ascosphaera apis contained in wax foundation can infect honeybee brood. Vet Microbiol 108:141–144.  https://doi.org/10.1016/j.vetmic.2005.03.005 CrossRefPubMedGoogle Scholar
  68. Food and Agriculture Organization of the United Nations (FAO) (2014) FAOSTAT, Rome. http://faostat.fao.org
  69. Forsgren E, de Miranda JR, Isaksson M et al (2009) Deformed wing virus associated with Tropilaelaps mercedesae infesting European honey bees (Apis mellifera). Exp Appl Acarol 47(2):87–97.  https://doi.org/10.1007/s10493-008-9204-4 CrossRefPubMedGoogle Scholar
  70. Forsgren E, Wei S, Guiling D et al (2015) Preliminary observations on possible pathogen spill-over from Apis mellifera to Apis cerana. Apidologie 46:265–275.  https://doi.org/10.1007/s13592-014-0320-3 CrossRefGoogle Scholar
  71. Friedmann H, Kern J (1956) The problem of cerophagy or wax-eating in the honey-guides. Q Rev Biol 31:19–30CrossRefGoogle Scholar
  72. Fries I (1988) Infectivity and multiplication of Nosema apis Z. in the ventriculus of the honey bee. Apidologie 19(3):319–328.  https://doi.org/10.1051/apido:19880310 CrossRefGoogle Scholar
  73. Fries I (1993) Nosema apis—a parasite in the honey bee colony. Bee World 74:5–19.  https://doi.org/10.1080/0005772X.1993.11099149 CrossRefGoogle Scholar
  74. Fries I, Feng F, da Silva A et al (1996a) Nosema ceranae n. sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur J Protistol 32:356–365.  https://doi.org/10.1016/S0932-4739(96)80059-9 CrossRefGoogle Scholar
  75. Fries I, Wei H, Wei S et al (1996b) Grooming behavior and damaged mites (Varroa jacobsoni) in Apis cerana cerana and Apis mellifera ligustica. Apidologie 27:3–12CrossRefGoogle Scholar
  76. Fries I, Hansen H, Imdorf A, Rosenkranz P (2003) Swarming in honey bees (Apis mellifera) and Varroa mite (Varroa destructor) population development in Sweden. Apidologie 34:1–9CrossRefGoogle Scholar
  77. Fries I, Chauzat M-P, Chen Y-P et al (2013) Standard methods for Nosema research. J Apic Res 52:1–28.  https://doi.org/10.3896/IBRA.1.52.1.14 CrossRefGoogle Scholar
  78. Fuchs S, Long L, Anderson D (2000) A scientific note on the genetic distinctness of Varroa mites on Apis mellifera L. and on Apis cerana Fabr. in North Vietnam. Apidologie 31:456–460CrossRefGoogle Scholar
  79. Garcia-Gonzalez E, Genersch E (2013) Honey bee larval peritrophic matrix degradation during infection with Paenibacillus larvae, the aetiological agent of American foulbrood of honey bees, is a key step in pathogenesis. Environ Microbiol 15:2894–2901PubMedGoogle Scholar
  80. Garg R, Sharma OP, Dogra GS (1984) Formic acid: an effective acaricide against Tropilaelaps clareae Delfinado and Baker (Laelaptidae: Acarina) and its effect on the brood and longevity of honey bees. Am Bee J 124:736–738Google Scholar
  81. Garrido C, Rosenkranz P, Paxton RJ et al (2003) Temporal changes in Varroa destructor fertility and haplotype in Brazil. Apidologie 34:535–541.  https://doi.org/10.1051/apido:2003041 CrossRefGoogle Scholar
  82. Gatehouse HS, Malone LA (1999) Genetic variability among Nosema apis isolates. J Apic Res 38:79–85CrossRefGoogle Scholar
  83. Genersch E (2010) American Foulbrood in honeybees and its causative agent, Paenibacillus larvae. J Invertebr Pathol 103:S10–S19.  https://doi.org/10.1016/j.jip.2009.06.015 CrossRefPubMedGoogle Scholar
  84. Gerson U, Dag A, Efrat C, Slabezki Y et al (1994) Tracheal mite, Acarapis woodi, comes to Israel. Israel Am Bee J 134:486Google Scholar
  85. Haddad NJ (2014) First detection of Nosema ceranae in Jordan. Eur Sci 10(33):1857–7881Google Scholar
  86. Hasemann L (1961) How long can spores of American foulbrood live? Am Bee J 101:298–299Google Scholar
  87. Heath LAF (1982) Chalk brood pathogens: a review. Bee World 63:130–135CrossRefGoogle Scholar
  88. Heath LAF (1985) Occurrence and distribution of chalkbrood disease of honeybees. Bee World 66:9–15.  https://doi.org/10.1080/0005772X.1985.11098816 CrossRefGoogle Scholar
  89. Hedtke K, Jensen PM, Jensen AB et al (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 CrossRefPubMedGoogle Scholar
  90. Hitchcock JD, Christensen M (1972) Occurrence of chalkbrood (Ascosphaera apis) in honey bees in the United States. Mycologia 64:1193–1198CrossRefGoogle Scholar
  91. Hoppe H, Ritter W, Stephen EWC (1989) The control of parasitic bee mites Varroa jacobsoni, Acarapis woodi and Tropilaelaps clareae with formic acid. Am Bee J 129:739–742Google Scholar
  92. Huang W, Jiang J, Chen Y et al (2007) A Nosema ceranae isolate from the honey bee Apis mellifera. Apidologie 38:30–37.  https://doi.org/10.1051/apido:2006054 CrossRefGoogle Scholar
  93. Huang W-F, Solter LF, Yau PM et al (2013) Nosema ceranae escapes fumagillin control in honey bees. PLoS Pathog 9:e1003185.  https://doi.org/10.1371/journal.ppat.1003185 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Hunter W, Ellis J, vanEngelsdorp D et al (2010) Large-scale field application of RNAi technology reducing Israeli Acute Paralysis Virus disease in honey bees (Apis mellifera, hymenoptera: Apidae). PLoS Pathog 6:e1001160.  https://doi.org/10.1371/journal.ppat.1001160 CrossRefPubMedPubMedCentralGoogle Scholar
  95. Ibay LA (1989) Biology of the two external Acarapis species of honey bees: Acarapis Dorsalis Morgenthaler and Acarapis Externus Morgenthaler (Acari: Tarsonemidae). Am Bee J 129:816Google Scholar
  96. Ken T, Hepburn HR, Radloff SE et al (2005) Heat-balling wasps by honeybees. Naturwissenschaften 92:492–495.  https://doi.org/10.1007/s00114-005-0026-5 CrossRefPubMedGoogle Scholar
  97. Khongphinitbunjong K, de Guzman LI, Burgett MD et al (2012) Behaviour response underpinning resistance and susceptibility of honey bees to Tropilaelaps mercedesae. Apidologie 43(5):590–599CrossRefGoogle Scholar
  98. Khongphinitbunjong K, de Guzman LI, Rinderer TE et al (2016) Responses of Varroa-resistant honey bees (Apis mellifera L.) to deformed wing virus. J Asia Pac Entomol 19:921–927.  https://doi.org/10.1016/j.aspen.2016.08.008 CrossRefGoogle Scholar
  99. Klee J, Besana AM, Genersch E et al (2007) Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol 96:1–10.  https://doi.org/10.1016/j.jip.2007.02.014 CrossRefPubMedGoogle Scholar
  100. Koeniger N, Koeniger G, De Guzman LI et al (1993) Survival of Euvarroa sinhai Delfinado and Baker (Acari, Varroidae) on workers of Apis cerana Fabr, Apis florea Fabr and Apis mellifera L in cages. Apidologie 24:403–410CrossRefGoogle Scholar
  101. Koeniger G, Koeniger N, Anderson DL et al (2002) Mites from debris and sealed brood cells of Apis dorsata colonies in Sabah (Borneo) Malaysia, including a new haplotype of Varroa jacobsoni. Apidologie 33:15–24CrossRefGoogle Scholar
  102. Kojima Y, Toki T, Morimoto T et al (2011) Infestation of Japanese native honey bees by tracheal mite and virus from non-native European honey bees in Japan. Microb Ecol 62:895–906.  https://doi.org/10.1007/s00248-011-9947-z CrossRefPubMedGoogle Scholar
  103. Kongpitak P, Polgár G, Heine J et al (2008) The efficacy of Bayvarol® and Check Mite® in the control of Tropilaelaps mercedesae in the European honey bee (Apis mellifera) in Thailand. Apıacta 43:12–16Google Scholar
  104. Kumar NR, Kumar R, Mbaya J et al (1993) Tropilaelaps-clareae found on Apis mellifera in Africa. Bee World 74:101–102CrossRefGoogle Scholar
  105. Laigo FM, Morse RA (1968) The mite Tropilaelaps clareae in Apis dorsata colonies in the Philippines. Bee World 49:116–118CrossRefGoogle Scholar
  106. Lanzi G, de Miranda JR, Boniotti MB et al (2006) Molecular and biological characterization of deformed wing virus of honeybees (Apis mellifera L.) J Virol 80:4998–5009CrossRefPubMedPubMedCentralGoogle Scholar
  107. Li J, Qin H, Wu J, Sadd BM et al (2012a) The prevalence of parasites and pathogens in Asian honeybees Apis cerana in China. PLoS One 7:e47955.  https://doi.org/10.1371/journal.pone.0047955 CrossRefPubMedPubMedCentralGoogle Scholar
  108. Li M, Chen H, Tang J et al (2012b) Characterization of nociceptive responses to bee venom-induced inflammation in neonatal rats. Brain Res 1472:54–62.  https://doi.org/10.1016/j.brainres.2012.07.005 CrossRefPubMedGoogle Scholar
  109. Lin RH, Sullivan J, Huang ZY (2001) Earlier foraging in Nosema-infected honey bee workers: are host Corpora allata needed. In: Abstract # D0616. Entomol Soc Am meeting abstracts. http://esa.confex.com/esa/2001/techprogram/programs.htm. Accessed 29 Sept 2017
  110. Liu TP (1991) Virus-like particles in the tracheal mite Acarapis woodi (Rennie). Apidologie 22:213–219CrossRefGoogle Scholar
  111. Liu ZL, Ho SH (1999) Bioactivity of the essential oil extracted from Evodia rutaecarpa Hook f. et Thomas against the grain storage insects, Sitophilus zeamais Motsch. and Tribolium castaneum (Herbst). J Stored Prod Res 35:317–328.  https://doi.org/10.1016/S0022-474X(99)00015-6 CrossRefGoogle Scholar
  112. Liu H, Pan G, Song S, Xu J et al (2008) Multiple rDNA units distributed on all chromosomes of Nosema bombycis. J Invertebr Pathol 99:235–238.  https://doi.org/10.1016/j.jip.2008.06.012 CrossRefPubMedGoogle Scholar
  113. Lo N, Gloag RS, Anderson DL, Oldroyd BP (2010) A molecular phylogeny of the genus Apis suggests that the giant Honeybee of the Philippines, A. breviligula Maa, and the plains Honeybee of southern India, A. indica Fabricius, are valid species. Syst Entomol 35(2):226–233CrossRefGoogle Scholar
  114. Locke B (2016) Natural Varroa mite-surviving Apis mellifera honeybee populations. Apidologie 47:467–482.  https://doi.org/10.1007/s13592-015-0412-8 CrossRefGoogle Scholar
  115. Mahmood R, Wagchoure ES, Raja S (2011) Effect of thymol and formic acid against ectoparasitic brood mite Tropilaelaps clareae in Apis mellifera colonies. Pak J Zool 43:91–95Google Scholar
  116. Mahmood R, Wagchoure ES, Ul Mohsin A et al (2012) Control of ectoparasitic mites in honeybee (Apis mellifera L.) colonies by using thymol and oxalic acid. Pak J Zool 44:985–989Google Scholar
  117. Martin S (1998) A population model for the ectoparasitic mite Varroa jacobsoni in honey bee (Apis mellifera) colonies. Ecol Model 109:267–281.  https://doi.org/10.1016/S0304-3800(98)00059-3 CrossRefGoogle Scholar
  118. Martin S, Holland K, Murray M (1997) Non-reproduction in the honeybee mite Varroa jacobsoni. Exp Appl Acarol 21:539–549CrossRefGoogle Scholar
  119. Martin SJ, Kemp D (1997) Average number of reproductive cycles performed by Varroa jacobsoni in honey bee (Apis mellifera) colonies. J Apic Res 36:113–123CrossRefGoogle Scholar
  120. Martin SJ, Highfield AC, Brettell L et al (2012) Global honey bee viral landscape altered by a parasitic mite. Science 336:1304–1306CrossRefGoogle Scholar
  121. Martín-Hernández R, Botías C, Barrios L et al (2011) Comparison of the energetic stress associated with experimental Nosema ceranae and Nosema apis infection of honeybees (Apis mellifera). Parasitol Res 109:605–612.  https://doi.org/10.1007/s00436-011-2292-9 CrossRefPubMedGoogle Scholar
  122. Matheson A (1993) World bee health report. Bee World 74:176–212.  https://doi.org/10.1080/0005772X.1993.11099183 CrossRefGoogle Scholar
  123. Mathpal Y (1984) Prehistoric rock paintings of bhimbetka. Abhinav Publications, New DelhiGoogle Scholar
  124. Matsuura M (1988) Ecological study on vespine wasps (Hymenoptera:Vespidae) attacking honeybee colonies: I. seasonal changes in the frequency of visits to apiaries by vespine wasps and damage inflicted, especially in the absence of artificial protection. Appl Entomol Zool 23(4):428–440.  https://doi.org/10.1303/aez.23.428 CrossRefGoogle Scholar
  125. Meikle WG, Sammataro D, Neumann P et al (2012) Challenges for developing pathogen-based biopesticides against Varroa destructor (Mesostigmata: Varroidae). Apidologie 43:501–514.  https://doi.org/10.1007/s13592-012-0118-0 CrossRefGoogle Scholar
  126. Michael DS (1957) Acarine disease found in India. Am Bee J 97:100Google Scholar
  127. Milne PS (1957) Acarine disease in Apis indica. Bee World 38:156.  https://doi.org/10.1080/0005772X.1957.11094995 CrossRefGoogle Scholar
  128. Mookhploy W, Kimura K, Disayathanoowat T et al (2015) Capsid gene divergence of Black Queen Cell Virus isolates in Thailand and Japan honey bee species. J Econ Entomol 108:1460–1464.  https://doi.org/10.1093/jee/tov102 CrossRefPubMedGoogle Scholar
  129. Mossadegh MS (1990) In vitro observations on ontogenesis of the mite, Euvarroa Sinhai Delfinado & Baker (Acari: Varroidae), in drone brood cells of the honeybee, Apis mellifera L. J Apic Res 29:230–232.  https://doi.org/10.1080/00218839.1990.11101224 CrossRefGoogle Scholar
  130. Mossadegh MS, Bahreini R (1994) Acarapis mites of honey-bee, Apis mellifera in Iran. Exp Appl Acarol 18:503–506.  https://doi.org/10.1007/BF00051472 CrossRefGoogle Scholar
  131. Munoz I, Garrido-Bailon E, Martin-Hernandez R et al (2008) Genetic profile of Varroa destructor infesting Apis mellifera iberiensis colonies. J Apic Res 47(4):310–313CrossRefGoogle Scholar
  132. Murray KD, Aronstein KA, de León JH (2007) Analysis of pMA67, a predicted rolling-circle replicating, mobilizable, tetracycline-resistance plasmid from the honey bee pathogen, Paenibacillus larvae. Plasmid 58:89–100.  https://doi.org/10.1016/j.plasmid.2007.02.001 CrossRefPubMedGoogle Scholar
  133. National Bureau of Agricultural Commodity and Food Standards (2008) Diagnosis of American foulbrood in bee. National Thai Agricultural Standard TAS 10351-2007, Royal Gazette Vol. 125 Special Section 3 D, 4 January B.E.2551. p 16Google Scholar
  134. Navajas M, Anderson DL, de Guzman LI et al (2010) New Asian types of Varroa destructor: a potential new threat for world apiculture. Apidologie 41:181–193CrossRefGoogle Scholar
  135. Oldroyd B, Wongsiri S (2006) Asian honey bees: biology, conservation, and human interactions. Harvard University Press, LondonGoogle Scholar
  136. Oldroyd BP, Wongsiri S, Seeley TD, Siriwat W (2006) Asian honey bees. (alk. paper) edn. Harvard University Press, CambridgeGoogle Scholar
  137. Ono M, Okada I, Sasaki M (1987) Heat production by balling in the Japanese honeybee, Apis cerana japonica as a defensive behavior against the hornet, Vespa simillima xanthoptera (Hymenoptera: Vespidae). Experientia 43:1031–1034.  https://doi.org/10.1007/BF01952231 CrossRefGoogle Scholar
  138. Otis GW, Kralj J (2001) Parasitic mites not present in North America. In: Webster TC, Delaplane KS (eds) Mites of the honey bee. Dadant, Hamilton, pp 251–272Google Scholar
  139. Oudemans AC (1904) On a new genus and species of parasitic Acari. Notes Leyden Mus 24(4):216–222Google Scholar
  140. Peng YS, Fang Y, Xu S et al (1987) The resistance mechanism of the Asian honey bee, Apis cerana Fabr., to an ectoparasitic mite, Varroa jacobsoni Oudemans. J Invertebr Pathol 49:54–60.  https://doi.org/10.1016/0022-2011(87)90125-X CrossRefGoogle Scholar
  141. Pernal SF, Clay H (2013) Honey bee diseases and pests. Canadian Association of Professional Apiculturists, Beaverlodge, AB, p 68Google Scholar
  142. Pettis JS et al (2013) A rapid survey technique for Tropilaelaps mite (Mesostigmata: Laelapidae) detection. J Econ Entomol 106:1535–1544CrossRefPubMedGoogle Scholar
  143. Qin X, Evans JD, Aronstein KA et al (2006) Genome sequences of the honey bee pathogens Paenibacillus larvae and Ascosphaera apis. Insect Mol Biol 15:715–718.  https://doi.org/10.1111/j.1365-2583.2006.00694.x CrossRefPubMedPubMedCentralGoogle Scholar
  144. Raffique MK, Mahmood R, Aslam M, Sarwar G (2012) Control of Tropilaelaps clareae mite by using formic acid and thymol in honey bee Apis mellifera L. colonies. Pak J Zool 44:1129–1135Google Scholar
  145. Ramsey SD (2018) Elucidation of novel nutritional, developmental, and behavioural adaptations for host exploitation in the mesostigmatid honey bee parasite Varroa destructor, Doctoral Dissertation, University of Maryland College Park, USGoogle Scholar
  146. Rashad SE, Eweis MA, Nour ME (1985) Studies on the infestation of honeybees (Apis mellifera) by Acarapis woodi in Egypt. pp 152–156Google Scholar
  147. Reynaldi FJ, López AC, Albo GN et al (2003) Differentiation of Ascosphaera apis isolates by rep-PCR fingerprinting and determination of chalkbrood incidence in Argentinean honey samples. J Apic Res 42:68–76.  https://doi.org/10.1080/00218839.2003.11101096 CrossRefGoogle Scholar
  148. Rice RN (2001) Nosema disease in honeybees: genetic variation and control. RIRDCGoogle Scholar
  149. Rosenkranz P, Kirsch R, Renz R (2006) Population dynamics of honey bee colonies and varroa tolerance: a comparison between Uruguay and Germany 7th Encontro sobre Abelhas, USP, Ribeirão Preto, BrazilGoogle Scholar
  150. Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103(Suppl 1):S96–S119.  https://doi.org/10.1016/j.jip.2009.07.016 CrossRefPubMedGoogle Scholar
  151. Royce LA, Krantz GW, Ibay LA et al (1988) Some observations on the biology and behavior of Acarapis woodi and Acarapis dorsalis in Oregon Africanized honey bees and bee mites/editors, Glen R Needham [et al]Google Scholar
  152. Sammataro D, Yoder J (2011) Global status of honey bee mites. In: Honey bee colony health: challenges and sustainable solutions. Contemporary topics in entomology. CRC Press, Boca Raton, pp 37–54CrossRefGoogle Scholar
  153. Sanpa S, Chantawannakul P (2009) Survey of six bee viruses using RT-PCR in Northern Thailand. J Invertebr Pathol 100:116–119CrossRefPubMedGoogle Scholar
  154. Shaw KE, Davidson G, Clark SJ et al (2002) Laboratory bioassays to assess the pathogenicity of mitosporic fungi to Varroa destructor (Acari: Mesostigmata), an ectoparasitic mite of the honeybee, Apis mellifera. Biol Control 24:266–276.  https://doi.org/10.1016/S1049-9644(02)00029-4 CrossRefGoogle Scholar
  155. Singh S (1961) Appearance of American foulbrood disease in Indian honeybee (Apis cerana indica Fabr.) Indian Bee J 27:46–50Google Scholar
  156. Solignac M 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 CrossRefPubMedPubMedCentralGoogle Scholar
  157. Steche W (1985) Revision of Zander & Bottcher. Nosematose. In: Krankheiten der Biene, Handbuch der BienenkundeGoogle Scholar
  158. Strauss U, Pirk CWW, Crewe RM et al (2015) Impact of Varroa destructor on honeybee (Apis mellifera Scutellata) colony development in South Africa. Exp Appl Acarol 65:89–106.  https://doi.org/10.1007/s10493-014-9842-7 CrossRefPubMedGoogle Scholar
  159. Takamatsu D, Morinishi K, Arai R, Sakamoto A, Okura M, Osaki M (2014) Typing of Melissococcus plutonius isolated from European and Japanese honeybees suggests spread of sequence types across borders and between different Apis species. Vet Microbiol 171:221–226CrossRefPubMedGoogle Scholar
  160. Thapa R, Wongsiri S (2003) Flying predators of the giant honey bees; Apis dorsata and Apis laboriosa in Nepal. Am Bee J 143:540–542Google Scholar
  161. Thapa R, Wongsiri S, Manandhar DN (2000) Current status of predators and diseases of honey bees in Nepal. In: Wongsiri S (ed) 7th IBRA and 5th AAA conf. Chiang Mai, Thailand, 2000. International Bee Research Association, CardiffGoogle Scholar
  162. Theantana T, Chantawannakul P (2008) Protease and β-N-acetylglucosaminidase of honey bee chalkbrood pathogen Ascosphaera apis. J Apic Res 47:68–76.  https://doi.org/10.1080/00218839.2008.11101426 CrossRefGoogle Scholar
  163. Traiyasut P, Mookhploy W, Kimura K et al (2016) First detection of honey bee viruses in wax moth. Chiang Mai J Sci 43:695–698Google Scholar
  164. Tsevegmid K, Neumann P, Yañez O (2016) The honey bee pathosphere of Mongolia: European viruses in Central Asia. PLoS One 11:e0151164.  https://doi.org/10.1371/journal.pone.0151164 CrossRefPubMedPubMedCentralGoogle Scholar
  165. Tutkun E, Maden S, Inci A et al (1993) General situation of chalkbrood disease in honeybees in Turkey. Turk Entomol Derg 17(2):65–68Google Scholar
  166. van der Zee R, Pisa L, Andonov S et al (2012) Managed honey bee colony losses in Canada, China, Europe, Israel and Turkey, for the winters of 2008–9 and 2009–10. J Apic Res 51:100–114.  https://doi.org/10.3896/IBRA.1.51.1.12 CrossRefGoogle Scholar
  167. Walter DE, Proctor HC (1999) Mites: ecology, evolution and behaviour (No. 639.089 W34). UNSW Press, SydneyGoogle Scholar
  168. Warrit N, Deborah Roan S, Chariya L (2006) Genetic subpopulations of Varroa mites and their Apis cerana hosts in Thailand. Apidologie 37:19–30CrossRefGoogle Scholar
  169. Whitaker J, Szalanski AL, Kence M (2011) Molecular detection of Nosema ceranae and N. apis from Turkish honey bees. Apidologie 42:174–180.  https://doi.org/10.1051/apido/2010045 CrossRefGoogle Scholar
  170. White GF (1913) Sacbrood, a disease of bees. US Department of Agriculture, Bureau of Entomology, Washington, DCGoogle Scholar
  171. Williams GR, Sampson MA, Shutler D et al (2008) Does fumagillin control the recently detected invasive parasite Nosema ceranae in Western honey bees (Apis mellifera)? J Invertebr Pathol 99:342–344.  https://doi.org/10.1016/j.jip.2008.04.005 CrossRefPubMedGoogle Scholar
  172. Williams GR, Shutler D, Little CM et al (2011) The microsporidian Nosema ceranae, the antibiotic Fumagilin-B®, and Western honey bee, Apis mellifera colony strength. Apidologie 42(1):15–22CrossRefGoogle Scholar
  173. Wongsiri S, Thapa R, Chantawannakul P et al (2005) Bee eating birds and honey bee predation in Thailand. Am Bee J 145:419–422Google Scholar
  174. Woyke J (1984) Survival and prophylactic control of Tropilaelaps clareae infesting Apis mellifera colonies in Afghanistan. Apidologie 15:421–434CrossRefGoogle Scholar
  175. Woyke J (1985) Further investigations into control of the parasite bee mite Tropilaelaps clareae without medication. J Apic Res 24:250–254.  https://doi.org/10.1080/00218839.1985.11100681 CrossRefGoogle Scholar
  176. Woyke J (1987) Length of stay of the parasitic mite Tropilaelaps clareae outside sealed honeybee brood cells as a basis for its effective control. J Apic Res 26:104–109CrossRefGoogle Scholar
  177. Wu J, Li J, Li JK (2006) Major honey plants and their utilization in China. Am Bee J 2:153–157Google Scholar
  178. Yang X, Cox-Foster DL (2005) Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proc Natl Acad Sci U S A 102:7470–7475.  https://doi.org/10.1073/pnas.0501860102 CrossRefPubMedPubMedCentralGoogle Scholar
  179. Yang B, Peng G, Li T, Kadowaki T (2013) Molecular and phylogenetic characterization of honey bee viruses, Nosema microsporidia, protozoan parasites, and parasitic mites in China. Ecol Evol 3:298–311.  https://doi.org/10.1002/ece3.464 CrossRefPubMedPubMedCentralGoogle Scholar
  180. Yen DF, Chyn LC (1971) Studies on a bacterial disease of honey bee in Taiwan. Plant Prot Bull 13:12–17Google Scholar
  181. Yoo KH, Lee Y, Gretzel U et al (2009) Trust in travel-related consumer generated media. In: Hopken W, Gretzel U, Law R (eds) Information and communication technologies in tourism 2009. Springer, New York, p 49e6Google Scholar
  182. Yoshiyama M, Kimura K (2011) Distribution of Nosema ceranae in the European honeybee, Apis mellifera in Japan. J Invertebr Pathol 106:263–267.  https://doi.org/10.1016/j.jip.2010.10.010 CrossRefPubMedGoogle Scholar
  183. Zander E (1909) Tierische Parasiten als Krankenheitserreger bei der Biene. Münch Bienenzeitung 31:196–204Google Scholar
  184. Zhang X, He SY, Evans JD, Pettis JS, Yin GF, Chen YP (2012) New evidence that deformed wing virus and black queen cell virus are multi-host pathogens. J Invertebr Pathol 109:156–159.  https://doi.org/10.1016/j.jip.2011.09.010 CrossRefPubMedGoogle Scholar
  185. Zhou T, Anderson D, Huang ZSH et al (2004) Identification of Varroa mites (Acari: Varroidae) infesting Apis cerana and Apis mellifera in China. Apidologie 35:645–654CrossRefGoogle Scholar
  186. Zioni N, Soroker V, Chejanovsky N (2011) Replication of Varroa destructor virus 1 (VDV-1) and a Varroa destructor virus 1–deformed wing virus recombinant (VDV-1–DWV) in the head of the honey bee. Virology 417:106–112CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Panuwan Chantawannakul
    • 1
    • 2
    • 3
  • Samuel Ramsey
    • 4
  1. 1.Department of Biology, Faculty of ScienceChiang Mai UniversityChiang MaiThailand
  2. 2.International College of Digital Innovation, Chiang Mai UniversityChiang MaiThailand
  3. 3.Environmental Science Research Center, Faculty of Science, Chiang Mai UniversityChiang MaiThailand
  4. 4.Department of EntomologyUniversity of MarylandCollege ParkUSA

Personalised recommendations