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The Asian Species of Apis

  • Sarah E. RadloffEmail author
  • H. R. Hepburn
  • Michael S. Engel
Chapter

Abstract

The history of the systematics of the Asian honeybee species is given, including discussions of paradigm shifts in the definition of species as earlier taxonomic methods evolved and were gradually replaced by an emphasis on populations, the statistical distributions of morphological characters and the reconstruction of evolutionary lineages. The limits of Asian species have been defined using principal component analysis, discriminant analysis, cluster analyses and nearest neighbour procedures, together with DNA characteristics, behaviour and nesting. This review presents a unified and coherent account of the Asian honeybees, based on the advances of the last three decades.

Keywords

Species Concept Morphometric Character Abdominal Tergite Biological Species Concept Mating Flight 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Aichholz R, Lorbeer E (1999) Investigation of combwax of honeybees with high-temperature gas chromatography and high-temperature gas chromatography-chemical ionization mass spectrometry. I. High-temperature gas chromatography. J Chromatogr A 855:601–615PubMedCrossRefGoogle Scholar
  2. Aichholz R, Lorbeer E (2000) Investigation of combwax of honeybees with high-temperature gas chromatography and high-temperature gas chromatography-chemical ionization mass spectrometry. II. High-temperature gas chromatography-chemical ionization mass spectrometry. J Chromatogr A 883:75–88PubMedCrossRefGoogle Scholar
  3. Alexander BA (1991) Phylogenetic analysis of the genus Apis (Hymenoptera: Apidae). Ann Entomol Soc Am 84:137–149Google Scholar
  4. Allen MF (1995) Bees and beekeeping in Nepal. Bee World 76:185–194Google Scholar
  5. Arias MC, Sheppard WS (2005) Phylogenetic relationships of honey bees (Hymenoptera: Apinae; Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol Phylogenet Evol 37:25–35PubMedCrossRefGoogle Scholar
  6. Arias MC, Tingek S, Kelitu A, Sheppard WS (1996) Apis nuluensis Tingek, Koeniger and Koeniger, 1996 and its genetic relationship with sympatric species inferred from DNA sequences. Apidologie 27:415–422CrossRefGoogle Scholar
  7. Baer B (2005) Sexual selection in Apis bees. Apidologie 36:187–200CrossRefGoogle Scholar
  8. Bhandari VC (1983) Biometrical studies on Apis florea F and Apis dorsata F of northwestern India. Thesis, Himachal Pradesh University, SimlaGoogle Scholar
  9. Blum MS, Fales HM, Morse RA, Underwood BA (2000) Chemical characters of two related species of giant honeybees (Apis dorsata and A. laboriosa): possible ecological significance. J Chem Ecol 26:801–807CrossRefGoogle Scholar
  10. Booncham U, Wongsiri S, Thirakupt K (1995) Niche differences between A. florea and A. andreniformis in dry-evergreen forest, Thailand. In: International Conference on Tropical Bees Environment, Pedu Lake, Kedah, p 33Google Scholar
  11. Chaiyawong T, Deowanish S, Wongsiri S, Sylvester HA, Rinderer TE, de Guzman L (2004) Multivariate morphometric study of Apis florea in Thailand. J Apic Res 43:123–127Google Scholar
  12. Chen YC (1993) Apiculture in China. Agricultural Scitech Publishing House of China, BeijingGoogle Scholar
  13. Cockerell TDA (1911) Descriptions and records of bees XXXV. Ann Mag Nat Hist 8:310–319Google Scholar
  14. Daly HV (1985) Insect morphometrics. Annu Rev Entomol 30:415–438CrossRefGoogle Scholar
  15. Damus MS, Otis GW (1997) A morphometric analysis of Apis cerana F. and Apis nigrocincta Smith populations from Southeast Asia. Apidologie 28:309–323CrossRefGoogle Scholar
  16. Deodikar GB (1959a) Geographical distribution based on morphological characters (structure of genitalia and crossability among different bee species). Indian Bee J 23:60–61Google Scholar
  17. Deodikar GB (1959b) Some taxonomic problems in honeybees. 1. The concept of supra-generic grouping. Bee World 40:121–124Google Scholar
  18. Deodikar GB (1960) Some indications on the phylogenetic interrelations among bees. Bee Genet Inf Bull 1:15–16Google Scholar
  19. Deodikar GB, Ghatge AL, Phadke RP, Mahindre DB, Kshirsagar K, Muvel KS, Thakar CV (1977) Nesting behaviour of Indian honeybees. III. Nesting behaviour of Apis dorsata Fab. Indian Bee J 39:1–12Google Scholar
  20. Diniz-Filho JAF, Malapsina O, Pignata MIB (1993) Geographic variation in Apis cerana indica F.: a spatial autocorrelation analysis of morphometric patterns. J Apic Res 32:65–72Google Scholar
  21. Dobzhansky TG (1937) Genetics and the origin of species. Columbia University Press, New YorkGoogle Scholar
  22. Dover C (1929) Wasps and bees in the Raffles Museum, Singapore. Bull Raffles’ Museum, Singapore 2:43–70Google Scholar
  23. Drory E (1888) From my notebook: notes on bees from a trip around the world. Bienenvater 20:20–30 [in German]Google Scholar
  24. Dung PX, Thai PH, Trung LQ (1996) Some comparative characteristics between Apis florea and Apis andreniformis in Minh Hai Province. In: Proceedings of the 3rd Asian apiculture association, Hanoi, p 62Google Scholar
  25. DuPraw EJ (1964) Non-Linnean taxonomy. Nature 202:849–852CrossRefGoogle Scholar
  26. Enderlein G (1906) New honeybees and contribution to the distribution of the genus Apis. Stett Entomol Ztg 67:331–334 [in German]Google Scholar
  27. Engel MS (1999) The taxonomy of recent and fossil honey bees (Hymenoptera: Apidae; Apis). J Hymenopt Res 8:165–196Google Scholar
  28. Engel MS (2006) A giant honey bee from the Middle Miocene of Japan (Hymenoptera: Apidae). Am Mus Novit 3504:1–12CrossRefGoogle Scholar
  29. Engel MS, Schultz TR (1997) Phylogeny and behavior in honey bees (Hymenoptera: Apidae). Ann Entomol Soc Am 90:43–53Google Scholar
  30. Engel MS, Hinojosa-Diaz IA, Rasnitsyn AP (2009) A honey bee from the Miocene of Nevada and the biogeography of Apis (Hymenoptera: Apidae; Apini). Proc Calif Acad Sci 60:23–38Google Scholar
  31. Fabricius JC (1787) Mantissa insectorum. Hafniae, Proft [in Latin, cited from Maa 1953]Google Scholar
  32. Fabricius JC (1793) Entomologia systematica emendata et aucta. Secundum classes, ordines, genera, species adjectis synonimis, locis, observationibus, descriptionibus. Hafniae, Proft [in Latin, cited from Maa 1953]Google Scholar
  33. Fuchs S, Koeniger N, Tingek S (1996) The morphometric position of Apis nuluensis Tingek, Koeniger and Koeniger, 1996 within cavity-nesting honeybees. Apidologie 27:397–405CrossRefGoogle Scholar
  34. Gan YY, Otis GW, Mardan MB, Tan SG (1991) Allozyme diversity in Asian Apis. In: Smith DR (ed) Diversity in the genus Apis. Westview, Boulder, pp 117–130Google Scholar
  35. Garnery L, Vautrin D, Cornuet JM, Solignac M (1991) Phylogenetic relationships in the genus Apis inferred from mitochondrial DNA sequence data. Apidologie 22:87–92CrossRefGoogle Scholar
  36. Gerstäcker CEA (1863) On the geographical distribution and varieties of the honeybee, with remarks upon the exotic honeybees of the old world. Ann Mag Nat Hist 11(270–283):333–347Google Scholar
  37. Goetze GKL (1964) The honeybee under natural and beekeeping conditions. Part 1. Systematics, reproduction and heritability. Monogr Angew Entomol 19:1–20 [in German]Google Scholar
  38. Hadisoesilo S, Otis GW (1996) Drone flight times confirm the species status of Apis nigrocincta Smith, 1861 to be a species distinct from Apis cerana F., 1793, in Sulawesi, Indonesia. Apidologie 27:361–369CrossRefGoogle Scholar
  39. Hadisoesilo S, Otis GW (1998) Differences in drone cappings of Apis cerana and Apis nigrocincta. J Apic Res 37:11–15Google Scholar
  40. Hadisoesilo S, Otis GW, Meixner M (1995) Two distinct populations of cavity-nesting honeybees (Hymenoptera: Apidae) in South Sulawesi, Indonesia. J Kans Entomol Soc 68:399–407Google Scholar
  41. Hadisoesilo S, Meixner M, Ruttner F (1999) Geographic variation within Apis koschevnikovi Buttel-Reepen, 1906, in Borneo. Treubia 31:299–306Google Scholar
  42. Hadisoesilo S, Raffiudin R, Susanti W, Atmowidi T, Hepburn C, Radloff SE, Fuchs S, Hepburn HR (2008) Morphometric analysis and biogeography of Apis koschevnikovi Enderlein (1906). Apidologie 39:495–503CrossRefGoogle Scholar
  43. Hepburn HR, Smith DR, Radloff SE, Otis GW (2001) Infraspecific categories of Apis cerana: morphometric, allozymal and mtDNA diversity. Apidologie 32:3–23.CrossRefGoogle Scholar
  44. Hepburn HR, Hepburn C (2005) Bibliography of Apis florea. Apidologie 36:377–378CrossRefGoogle Scholar
  45. Hepburn HR, Hepburn C (2008) Bibliography of Apis koschevnikovi. Apidologie 39:507Google Scholar
  46. Hepburn HR, Hepburn C (2009) Bibliography of Apis andreniformis. Apidologie 40:3CrossRefGoogle Scholar
  47. Hepburn HR, Smith DR, Radloff SE, Otis GW (2001a) Infraspecific categories of Apis cerana: morphometric, allozymal and mtDNA diversity. Apidologie 32:3–23CrossRefGoogle Scholar
  48. Hepburn HR, Radloff SE, Verma S, Verma LR (2001b) Morphometric analysis of Apis cerana populations in the southern Himalayan region. Apidologie 32:435–447CrossRefGoogle Scholar
  49. Hepburn HR, Radloff SE, Otis GW, Fuchs S, Verma LR, Ken T, Chaiyawong T, Tahmasebi G, Ebadi R, Wongsiri S (2005) Apis florea: morphometrics, classification and biogeography. Apidologie 36:359–376CrossRefGoogle Scholar
  50. Huxley J (1940) The new systematics. Clarendon, OxfordGoogle Scholar
  51. Jain PC (1967) Morphometrics of bees Apis dorsata F., Apis indica F., Apis florea F., Megachile lanata F., Trigona smithii B. (Hymenoptera: Apidae) and their foraging habits at Udaipur. Thesis, University of UdaipurGoogle Scholar
  52. Jayavasti S, Wongsiri S (1992) Scanning electron microscopy analysis of honeybees (Apis florea, Apis dorsata, Apis cerana, Apis mellifera, Apis andreniformis and Apis koschevnikovi) stings. Recent Adv Toxicol Res 2:193–204Google Scholar
  53. Keeling CI, Otis GW, Hadisoesilo S, Slessor KN (2001) Mandibular gland component analysis in the head extracts of Apis cerana and Apis nigrocincta. Apidologie 32:243–252CrossRefGoogle Scholar
  54. Kirchner WH, Dreller C, Grasser A, Baidya D (1996) The silent dances of the Himalayan honeybee, Apis laboriosa. Apidologie 27:331–339CrossRefGoogle Scholar
  55. Koeniger G (1991) Diversity in Apis mating systems. In: Smith DR (ed) Diversity in the genus Apis. Westview, Boulder, pp 199–212Google Scholar
  56. Koeniger N, Koeniger G (1991) An evolutionary approach to mating behaviour and drone copulatory organs in Apis. Apidologie 22:581–590CrossRefGoogle Scholar
  57. Koeniger N, Koeniger G (2000) Reproductive isolation among species of the genus Apis. Apidologie 31:313–339CrossRefGoogle Scholar
  58. Koeniger N, Koeniger G (2001) Behavioural mating barriers among sympatric species of the genus Apis. In: Proceedings of the 7th international conference on apiculture tropical bees, Chiang Mai, pp 79–85Google Scholar
  59. Koeniger N, Koeniger G, Gries M, Tingek S, Kelitu A (1996a) Observations on colony defense of Apis nuluensis Tingek, Koeniger and Koeniger, 1996 and predatory behaviour of the hornet, Vespa multimaculata Pérez, 1910. Apidologie 27:341–352CrossRefGoogle Scholar
  60. Koeniger N, Koeniger G, Gries M, Tingek S, Kelitu A (1996b) Reproductive isolation of Apis nuluensis Tingek, Koeniger and Koeniger, 1996 by species-specific mating time. Apidologie 27:353–360CrossRefGoogle Scholar
  61. Koeniger N, Koeniger G, Tingek S, Kelitu A (1996c) Interspecific rearing and acceptance of queens between Apis cerana Fabricius, 1793 and Apis koschevnikovi Buttel-Reepen, 1906. Apidologie 27:371–380CrossRefGoogle Scholar
  62. Koschevnikov GA (1900–1905) Materials on the natural history of the honeybee. Soc Amateurs Sci Nat 1–2 [cited from Alapatov 1929]Google Scholar
  63. Kshirsagar KK (1969) Preliminary observations on the biometry of Apis dorsata Fab. queen. Indian Bee J 31:12–16Google Scholar
  64. Kuang BY (1983) Studies on the small black honeybee. Chin Apic 6:10 [in Chinese]Google Scholar
  65. Kuang BY (1986) The species of Apis in China. Apic China 5:7–9 [in Chinese]Google Scholar
  66. Kuang BY (2002) Evolution and classification of Apini. J Bee 2:1–2 [in Chinese]Google Scholar
  67. Kuang BY, Li YC (1985) The genus Apis in China. Chinese Beekeep 76:7–9 [in Chinese]Google Scholar
  68. Kuang BY, Li YO (1988) Studies on Apini. Sci Agric Sinica 21:85–90 [in Chinese]Google Scholar
  69. Lavrekhin FA (1935) Contribution to the study of variation of the honeybee. 2. Comparative biometric characteristics of the sexual appendages of the drones belonging to different forms of the genus Apis. Zool Zh 14:655–663 [in Russian]Google Scholar
  70. Li S, Meng YP, Chang JT, Li JH, He SY, Kuang BY (1986) A comparative study of esterase isozymes in 6 species of Apis and 9 genera of Apoidea. J Apic Res 25:129–133Google Scholar
  71. Li YQ (1984) Discussions on the taxonomy of six species of Apis. J Bee 4:19–21 [in Chinese]Google Scholar
  72. Linnaeus C (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Salviae Holmiae Stockholm [in Latin, cited from Maa 1953]Google Scholar
  73. Lo NH, Gloag RS, Snderson DL, Oldroyd BP (2010) A molecular phylogeny of the genus Apis suggests that the Giant Honey Bee of the Philippines, A. breviligula Maa, and the Plains Honey Bee of southern India, A. indica Fabricius, are valid species. Syst Entomol 35:226–233CrossRefGoogle Scholar
  74. Maa T (1953) An inquiry into the systematics of the tribus Apidini or honeybees (Hym.). Treubia 21:525–640Google Scholar
  75. Mathew S, Mathew K (1988) The ‘red’ bees of Sabah. Newsl Beekeep Trop Subtrop Countries 12:10Google Scholar
  76. Mayr E (1942) Systematics and the origin of species. Columbia University Press, New YorkGoogle Scholar
  77. McEvoy MV, Underwood BA (1988) The drone and species status of the Himalayan honeybee, Apis laboriosa (Hymenoptera: Apidae). J Kans Entomol Soc 61:246–249Google Scholar
  78. Mogga J, Ruttner F (1988) Apis florea in Africa: source of the founder population. Bee World 69:100–103Google Scholar
  79. Morse RA, Laigo FM (1968) Honeybees in the Philippines. Philipp Biota 3:3–4Google Scholar
  80. Mujumdar S, Kshirsagar KK (1986) Morphometric characterization of Apis dorsata Fabr. workers. Indian Bee J 48:25–29Google Scholar
  81. Muzaffar N, Ahmad R (1989) Distribution and competition of Apis spp. in Pakistan. In: Proceedings of the 4th international conference on apiculture in tropical climates, Cairo, pp 449–452Google Scholar
  82. Nanork P, Deowanish S, Wongsiri S (2001) Mitochondrial DNA variability of dwarf honeybee (Apis florea Fabricius (1787)) in Thailand by using PCR-RFLP technique. In: Proceedings of the 7th international conference on tropical bees, Chiang Mai, pp 341–345Google Scholar
  83. Narayanan ES, Sharma PL, Phadke KG (1960) Studies on biometry of the Indian bees II. Tongue length, wing hooks, worker-brood-cell size and thickness of comb of Apis florea F. at Pusa (Bihar). Indian Bee J 22:81–88Google Scholar
  84. Nunamaker RA, Wilson WT, Ahmad R (1984) Malate dehydrogenase and non-specific esterase isoenzymes of Apis florea, A. dorsata, and A. cerana detected by isoelectric focusing. J Kans Entomol Soc 57:591–595Google Scholar
  85. Oldroyd BP, Rinderer TE, Wongsiri S (1992) Pollen resource partitioning by Apis dorsata, Apis cerana, Apis andreniformis and Apis florea in Thailand. J Apic Res 31:3–7Google Scholar
  86. Ono M (1992) The Asian honeybees (Apis spp.). Honeybee Sci 13:19–22Google Scholar
  87. Otis GW (1991) A review of the diversity of species within Apis. In: Smith DR (ed) Diversity in the genus Apis. Westview, Boulder, pp 29–49Google Scholar
  88. Otis GW (1996) Distributions of recently recognized species of honeybees (Hymenoptera: Apidae; Apis) in Asia. J Kans Entomol Soc 69:311–333Google Scholar
  89. Otis GW, Hadisoesilo S (1990) Honeybee survey of South Sulawesi. J Penelitian Kehutanan 4:1–3Google Scholar
  90. Otis GW, Hadisoesilo S, Sugiyani, Cooper AM (2001) Using social bees as indicators of habitat quality in Sulawesi, Indonesia. In: Proceedings of the 7th international conference on tropical bees, Chiang Mai, pp 313–317Google Scholar
  91. Özkani A, Gharlek MM, Özden B, Kandemir I (2009) Multivariate morphometric study on Apis florea distributed in Iran. Turk J Zool 33:93–102Google Scholar
  92. Patinawin S, Wongsiri S (1993) Male genitalia of honey bees. In: Connor LJ, Rinderer TE, Sylvester HA, Wongsiri S (eds) Asian apiculture. Wicwas, Cheshire, Connecticut, pp 110–116Google Scholar
  93. Peng YS, Nasr ME, Locke SJ (1989) Geographical races of Apis cerana Fabricius in China and their distribution. Review of recent Chinese publications and a preliminary statistical analysis. Apidologie 20:9–20CrossRefGoogle Scholar
  94. Pesenko YA, Lelei AS, Radchenko VG, Filatkin GN (1989) Chinese wax-bee, Apis cerana cerana F. (Hymenoptera: Apidae) in the Far East of the USSR. Entomol Obozr 68:527–548 [in Russian]Google Scholar
  95. Petrov P (1992) Distribution and phylogeny of the honeybee genus Apis (Hymenoptera: Apidae). Uspekhi Sovremennoi Biologii 112:359–372 [in Russian]Google Scholar
  96. Poulton EB (1908) Essays on evolution. Clarendon, OxfordGoogle Scholar
  97. Radloff SE, Hepburn HR (1998) The matter of sampling distance and confidence levels in the subspecific classification of honeybees, Apis mellifera L. Apidologie 29:491–501CrossRefGoogle Scholar
  98. Radloff SE, Hepburn HR (2000) Population structure and morphometric variance in the Apis mellifera scutellata group of honeybees in Africa. Genet Mol Biol 23:305–316CrossRefGoogle Scholar
  99. Radloff SE, Hepburn HR (2002) Multivariate morphometric analysis of the Apis cerana populations of southern Asia. In: Proceedings of the 14th international congress, IUSSI, Sapporo, p 209Google Scholar
  100. Radloff SE, Hepburn HR, Otis GW (2001) Flight machinery of honey bees (Hymenoptera: Apidae; Apis). In: Proceedings of the 7th international conference on tropical bees, Chiang Mai, pp 163–168Google Scholar
  101. Radloff SE, Hepburn HR, Koeniger G (2003a) Comparison of flight design of Asian honeybee drones. Apidologie 34:353–358CrossRefGoogle Scholar
  102. Radloff SE, Hepburn HR, Bangay L (2003b) Quantitative analysis of intercolonial and intracolonial morphometric variance in honeybees, Apis mellifera and Apis cerana. Apidologie 34:339–352CrossRefGoogle Scholar
  103. Radloff SE, Hepburn HR, Fuchs S (2005a) The morphometric affinities of Apis cerana of the Hindu Kush and Himalayan regions of western Asia. Apidologie 36:25–30CrossRefGoogle Scholar
  104. Radloff SE, Hepburn HR, Hepburn C, Fuchs S, Otis GW, Sein MM, Aung HL, Pham HT, Tam DQ, Nuru A, Tan K (2005b) Multivariate morphometric analysis of the Apis cerana populations of mainland southern Asia. Apidologie 36:127–139CrossRefGoogle Scholar
  105. Radloff SE, Hepburn HR, Fuchs S, Otis GW, Hadisoesilo S, Hepburn C, Ken T (2005c) Multivariate morphometric analysis of the Apis cerana populations of oceanic Asia. Apidologie 36:475–492CrossRefGoogle Scholar
  106. Radloff SE, Hepburn C, Hepburn HR, Fuchs S, Hadisoesilo S, Tan K, Engel MS, Kuznetsov V (2010) Population structure and classification of Apis cerana. Apidologie 41:589–601Google Scholar
  107. Raffiudin R, Crozier RH (2007) Phylogenetic analysis of honeybee behavioral evolution. Mol Phylogenet Evol 43:543–552PubMedCrossRefGoogle Scholar
  108. Ratnam R (1939) A preliminary study in the biometric variations in the Indian honeybees. Madras Agric J 27:432–439Google Scholar
  109. Rattanawannee A, Channchao C, Wongsiri S (2008) Morphometric and genetic variation of small dwarf honeybees Apis andreniformis Smith, 1858 in Thailand. Insect Sci 14:451–460CrossRefGoogle Scholar
  110. Rensch B (1929) The concept of geographical races and the problem of speciation. Gebrüder Borntraeger, Berlin [in German]Google Scholar
  111. Rinderer TE (1988) The rediscovery of Apis koschevnikovi. Am Bee J 128:807Google Scholar
  112. Rinderer TE, Koeniger N, Tingek S, Mardan M, Koeniger G (1989) A morphological comparison of the cavity dwelling honeybees of Borneo Apis koschevnikovi (Buttel-Reepen, 1906) and Apis cerana (Fabricius, 1793). Apidologie 20:405–411CrossRefGoogle Scholar
  113. Rinderer TE, Oldroyd BP, Wongsiri S, Sylvester HA, de Guzman LI, Potichot S, Sheppard WS, Buchmann SL (1993) Time of drone flight in four honeybee species in south-eastern Thailand. J Apic Res 32:27–33Google Scholar
  114. Rinderer TE, Oldroyd BP, Wongsiri S, Sylvester HA, de Guzman LI, Stelzer JA, Riggio RM (1995) A morphological comparison of the dwarf honeybees of southeastern Thailand and Palawan, Philippines. Apidologie 26:387–394CrossRefGoogle Scholar
  115. Rinderer TE, Wongsiri S, Kuang BY, Liu JS, Oldroyd BP, Sylvester HA, de Guzman LI (1996) Comparative nest architecture of the dwarf honeybees. J Apic Res 35:19–26Google Scholar
  116. Rinderer TE, Oldroyd BP, de Guzman LI, Wattanachaiyingcharoen W, Wongsiri S (2002) Spatial distribution of the dwarf honeybees in an agroecosystem in southeastern Thailand. Apidologie 33:539–543CrossRefGoogle Scholar
  117. Roubik DW, Sakagami SF, Kudo I (1985) A note on distribution and nesting of the Himalayan honeybee Apis laboriosa Smith (Hymenoptera: Apidae). J Kans Entomol Soc 58:746–749Google Scholar
  118. Ruttner F (1975) A metatarsal clasping structure in the Apis drone. Entomol Germ 2:22–29Google Scholar
  119. Ruttner F (1988) Biogeography and taxonomy of honeybees. Springer, BerlinGoogle Scholar
  120. Ruttner F (1992) Naturgeschichte der Honigbienen. Ehrenwirth, MunchenGoogle Scholar
  121. Ruttner F, Kauhausen D, Koeniger N (1989) Position of the red honey bee, Apis koschevnikovi (Buttel-Reepen 1906), within the genus Apis. Apidologie 20:395–404CrossRefGoogle Scholar
  122. Sakagami SF, Matsumura T, Ito K (1980) Apis laboriosa in the Himalaya, the little known world largest honeybee (Hymenoptera: Apidae). Insecta Matsumurana 19:47–77Google Scholar
  123. Sakai S, Hoshiba H, Hoshiba E (1986) Integrated taxonomic information on honeybees. In: Proceedings of the 30th International Congress Apicultural, Nagoya, pp 134–139Google Scholar
  124. Sharma PC (1983) Morphometric studies on Apis florea F. and Apis dorsata F. of Himachal Pradesh and Punjab. Thesis, Himachal Pradesh UniversityGoogle Scholar
  125. Sheppard WS, Berlocher SH (1989) Allozyme variation and differentiation among four Apis species. Apidologie 20:419–431CrossRefGoogle Scholar
  126. Singh MP, Verma LR, Daly HV (1990) Morphometric analysis of the Indian honeybee in the northeast Himalayan region. J Apic Res 29:3–14Google Scholar
  127. Smith DR (1991) Mitochondrial DNA and honeybee biogeography. In: Smith DR (ed) Diversity in the genus Apis. Westview, Boulder, pp 131–176Google Scholar
  128. Smith DR (2002) Biogeography of Apis cerana: Southeast Asia and the Indo-Pakistan subcontinent. In: Proceedings of the 16th international congress, IUSSI, Sapporo, p 209Google Scholar
  129. Smith DR, Villafuerte L, Otis G, Palmer MR (2000) Biogeography of Apis cerana F. and A. nigrocincta Smith: Insights from mtDNA studies. Apidologie 31:265–280CrossRefGoogle Scholar
  130. Smith DR, Palmer MR, Otis GW, Damus M (2003) Mitochondrial DNA and AFLP markers support species status of Apis nigrocincta. Insectes Soc 50:185–190CrossRefGoogle Scholar
  131. Smith F (1858) Catalogue of the hymenopterous insects collected at Sarawak, Borneo; Mount Ophir, Malacca; and at Singapore, by A.R. Wallace. Proc Linn Soc Lond 2:42–130Google Scholar
  132. Smith F (1861) Descriptions of new species of hymenopterous insects collected by A.R. Wallace at Celebes. Proc Linn Soc Lond 5:57–93Google Scholar
  133. Smith F (1865) On the species and varieties of the honey-bees belonging to the genus Apis. Ann Mag Nat Hist 15:372–380Google Scholar
  134. Smith F (1871) A catalogue of the aculeate Hvmenoptcra and Ichneumonidae of India and the eastern Archipelago. J Linn Soc 11:285–415CrossRefGoogle Scholar
  135. Sulistianto A (1990) Morphometric analysis of Indonesian honeybees. Thesis, University of Wales College, CardiffGoogle Scholar
  136. Sylvester HA, Limbipichai K, Wongsiri S, Rinderer TE, Mardan MB (1998) Morphometric studies of Apis cerana in Thailand and the Malaysian peninsula. J Apic Res 37:137–145Google Scholar
  137. Szabo TI (1990) Morphometric characteristics of Apis cerana from Sri Lanka. Apidologie 21:505–509CrossRefGoogle Scholar
  138. Tahmasebi G, Ebadi R, Tajabadi N, Akhoundi M, Faraji S (2002) The effects of geographical and climatic conditions on the morphological variation and separation of Iranian small honeybee (Apis florea F.) populations. J Sci Tech Agric Nat Res 6:169–176Google Scholar
  139. Takahashi JI, Nakamura J, Sasaki M, Tingek S, Akimoto SI (2002) New haplotypes for the non-coding region of mitochondrial DNA in cavity-nesting honey bees Apis koschevnikovi and Apis nuluensis. Apidologie 33:25–31CrossRefGoogle Scholar
  140. Tan K, Fuchs S, Ruiguang Z (2002) Morphometrical characterization of Apis cerana in Yunnan Province of China. In: Proceedings of the 14th international congress, IUSSI, Sapporo, p 208Google Scholar
  141. Tan K, Fuchs S, Koeniger N, Ruiguang Z (2003) Morphological characterization of Apis cerana in the Yunnan province of China. Apidologie 34:553–561CrossRefGoogle Scholar
  142. Tanaka H, Roubik DW, Kato M, Liew F, Gunsalam G (2001) Phylogenetic position of Apis nuluensis of northern Borneo and phylogeography of A. cerana as inferred from mitochondrial DNA sequences. Insectes Soc 48:44–51CrossRefGoogle Scholar
  143. Thakar CV, Tonapi KV (1962) Nesting behaviour of Indian honeybees. II. Nesting habits and comb cell differentiation in Apis florea Fab. Indian Bee J 24:27–31Google Scholar
  144. Thapa R, Shrestha R, Manandhar DN, Bista S, Kafle B (2001) Beekeeping in Nepal. In: Proceedings of the 7th international conference on tropical bees, Chiang Mai, pp 409–413Google Scholar
  145. Tilde AC, Fuchs S, Koeniger N, Cervancia CR (2000) Morphometric diversity of Apis cerana Fabr. within the Philippines. Apidologie 31:249–264CrossRefGoogle Scholar
  146. Tingek S, Mardan M, Rinderer TE, Koeniger N, Koeniger G (1988) Rediscovery of Apis vechti (Maa, 1953): the Saban honey bee. Apidologie 19:97–102CrossRefGoogle Scholar
  147. Tingek S, Koeniger G, Koeniger N (1996) Description of a new cavity-nesting species of Apis (Apis nuluensis n. sp.) from Sabah, Borneo, with notes on its occurrence and reproductive biology. Senckenbergiana Biol 76:115–119Google Scholar
  148. Trehan KN, Singh H (1961) Measurements of the tongue and of the worker and drone cells of Apis dorsata Fab. in the Punjab. Indian Bee J 23:31–36Google Scholar
  149. Trung LQ, Dung PX, Ngan TX (1996) A scientific note on first report of Apis laboriosa F Smith, 1871 in Vietnam. Apidologie 27:487–488CrossRefGoogle Scholar
  150. Underwood BA (1990) The behavior and energetics of high-altitude survival by the Himalayan honeybee, Apis laboriosa. Thesis, Cornell University, IthacaGoogle Scholar
  151. Verma LR (1992) Species and genetic diversity in Himalayan honeybees. In: Verma LR (ed) Honeybees in mountain agriculture. Oxford and IBH, New Delhi, pp 39–49Google Scholar
  152. Verma LR, Mattu VK, Daly HV (1994) Multivariate morphometrics of the Indian honeybee in the northwest Himalayan region. Apidologie 25:203–223CrossRefGoogle Scholar
  153. von Buttel-Reepen H (1906) Contributions to the systematics, biology as well as the historical and geographical distribution of honeybees (Apis mellifica L.) their variability and other Apis species. Mitt Zool Mus Berlin 3:117–201 [in German]Google Scholar
  154. Wheeler QD, Meier R (eds) (2000) Species concepts and phylogenetic theory. Columbia University Press, New YorkGoogle Scholar
  155. Willis LG, Winston ML, Honda BM (1992) Phylogenetic relationships in the honeybee (genus Apis) as determined by the sequence of the cytochrome oxidase II region of mitochondrial DNA. Mol Phylogenet Evol 1:169–178PubMedCrossRefGoogle Scholar
  156. Wilson EO, Brown WL (1951) The subspecies concept and its taxonomic implication. Syst Zool 2:97–111CrossRefGoogle Scholar
  157. Wongsiri S, Limbipichai K, Tangkanasing P, Mardan M, Rinderer TE, Sylvester HA, Koeniger G, Otis GW (1990) Evidence of reproductive isolation confirms that Apis andreniformis (Smith, 1858) is a separate species from sympatric Apis florea (Fabricius, 1787). Apidologie 21:47–52CrossRefGoogle Scholar
  158. Woyke J, Wilde J, Wilde M, Sivaram V, Cervancia C, Nagaraja N, Reddy M (2008) Comparison of defense body movements of Apis laboriosa, Apis dorsata dorsata and Apis dorsata breviligula honey bees. J Insect Behav 21:481–494CrossRefGoogle Scholar
  159. Wu YR, Kuang B (1986) A study of the genus Micrapis (Apidae). Zool Res 7:99–102 [in Chinese]Google Scholar
  160. Wu YR, Kuang B (1987) Two species of small honeybee: a study of the genus Micrapis. Bee World 68:153–155Google Scholar
  161. Yang GH (1986) The distribution of the eastern honeybee (Apis cerana Fab.) in China and an analysis of its subspecies. J Yunnan Agric Univ 12:202–206 [in Chinese]Google Scholar
  162. Yang GH (2001) The biology of Apis cerana. GH Yang, Beijing [in Chinese]Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  • Sarah E. Radloff
    • 1
    Email author
  • H. R. Hepburn
    • 2
  • Michael S. Engel
    • 3
  1. 1.Department of StatisticsRhodes UniversityGrahamstownSouth Africa
  2. 2.Department of Zoology and EntomologyRhodes UniversityGrahamstownSouth Africa
  3. 3.Division of Entomology, Natural History MuseumUniversity of KansasLawrenceUSA

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