Comparative reproductive biology of honeybees

Honeybees of Asia

Volumn , Issue , 2011, Pages 159-206

  Koeniger, Gudrun ^a   Koeniger, Nikolaus ^a   Phiancharoen, Mananya ^b  

^a GOETHE UNIVERSITY   (Germany)

^b KING MONGKUT'S UNIVERSITY OF TECHNOLOGY THONBURI   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84874513972     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-642-16422-4_8     Document Type: Chapter

References (130)

1. Adams J, Rothman ED, Kerr WE, Paulino ZL (1977) Estimation of sex alleles and queen matings from diploid male frequencies in a population of A. mellifera. Genetics 86:583-596
2. Allen MD (1965) The effect of a plentiful supply of drone comb on colonies of honeybees. J Apic Res 4:109-119
3. Baer B, Heazlewood JL, Taylor NL, Eubel H, Millar AH (2009) The seminal fluid proteome of the honeybee Apis mellifera. Proteomics 9:2085-2097
4. Baudry E, Solignac M, Garnery L, Gries M, Cornuet JM, Koeniger N (1998) Relatedness among honeybees (Apis mellifera) of a drone congregation. Proc R Soc Lond B 265:2009-2014
5. Buawangpang N, Sukumalanand P, Burgett M (2009) Apis florea drone flight: longevity and flight performance. Apidologie 40:20-25
6. Burgett DM, Titayavav M, Sukumalonand P (2007) The drone mating flight of the eastern honeybee (A. cerana F.): duration, temporal period and inter-flight period. Nat Hist Bull Siam Soc 55:99-104
7. Camargo JMF (1972) Preliminary notes on the reproductive system of Apis dorsata and A. florea queens. In: Anonymous (ed) Homeuagem à Warwick E Kerr. Faculdade de Filosofia. Ciências e Letras, Rio Claro, pp 47-56 [in Portuguese]
8. Camargo JMF, Mello MLS (1970) Anatomy and histology of the genital tract, spermatheca, spermathecal duct and glands of Apis mellifica queens (Hymenoptera: Apidae). Apidologie 1:351-374
9. Collins AM, Caperna TJ, Williams V, Garett WM, Evans JD (2006) Proteomic analyses of male contributions to honeybee sperm storage and mating. Insect Mol Biol 15:541-549
10. Crozier RH, Pamilo P (1996) Evolution of social insect colonies: sex allocation and kin selection. Oxford University Press, Oxford
11. Drescher W (1969) Die Flugaktivität von Drohnen der Rasse Apis mellifera carnica und Apis mellifera ligustica in Abhängigkeit von Lebensalter und Witterung. Z Bienenforsch 9:390-409 [in German]
12. Esslen J, Kaissling KE (1976) Zahl und Verteilung antennaler Sensillen bei der Honigbiene (Apis mellifera L.). Zoomorphologie 83:227-251 [in German]
13. Franck P, Koeniger N, Lahner G, Crewe R, Solignac M (2000) Evolution of extreme polyandry: an estimate of mating frequency in two African honeybee subspecies, A. mellifera monticola and A. mellifera scutellata. Insectes Soc 47:364-370
14. Franck P, Solignac M, Vautrin D, Cornuet JM, Koeniger G, Koeniger N (2002) Sperm competition and last-male precedence in the honeybee. Anim Behav 64:503-509
15. Frisch B, Koeniger N (1994) Social synchronisation of the activity rhythms of honeybees within the colony. Behav Ecol Sociobiol 35:91-98
16. Fuchs S, Moritz RFA (1998) Evolution of extreme polyandry in the honeybee Apis mellifera L. Behav Ecol Sociobiol 9:269-275
17. Fujiwara S, Miura H, Kumagai T, Sawaguchi T, Naya S, Goto KT, Suzuki K (1994) Drone congregation of Apis cerana japonica in an open area over larger trees (Zelkovia serrata). Apidologie 25:331-337
18. Gary NE (1962) Chemical mating attractants in the queen honeybee. Science 136:773-774
19. Gerstung F (1910) der Bien und sein Zucht. Fritz Pfenningstorff, Berlin [in German]
20. Gessner B, Ruttner F (1977) Transfer der Spermien in die Spermatheka der Bienenkönigin. Apidologie 8:1-18 [in German]
21. Gries M (1997) Vergleichende Untersuchungen zum Flugverhalten von Drohnen der Gattung Apis bei der Königinnenverfolgung. Thesis, Universität Frankfurt am Main [in German]
22. Gries M, Koeniger N (1996) Straight forward to the queen: pursuing honeybee drones (Apis mellifera L.) adjust their body axis to the direction of the queen. J Comp Physiol A 179:539-544
23. 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 27:361-369
24. Hölldobler B, Wilson EO (2009) The superorganism, the beauty, elegance and strangeness of insect societies. W. W. Norton, New York
25. Klenk M, Koeniger G, Koeniger N, Fasold F (2004) Proteins in spermathecal gland secretion and spermathecal fluid and the properties of a 29 kDa protein in queens of A. mellifera. Apidologie 35:371-381
26. Koeniger N (1970) Über die Fähigkeit der Bienenkönigin (A. mellifera L.) zwischen Arbeiterinnen- und Drohnenzellen zu unterscheiden. Apidologie 1:115-142 [in German]
27. Koeniger G (1986) Mating sign and multiple mating in the honeybee. Bee World 67:141-150
28. Koeniger G (1990) The role of mating sign in honey bees, Apis mellifera L.: does it hinder or promote multiple mating? Anim Behav 39:444-449
29. Koeniger N, Koeniger G (1991) An evolutionary approach to mating behaviour and drone copulatory organs in Apis. Apidologie 22:581-590
30. Koeniger N, Koeniger G (2000) Reproductive isolation among species of the genus Apis. Apidologie 31:313-339
31. Koeniger N, Koeniger G (2007) Mating flight duration of Apis mellifera queens: As short as possible, as long as necessary. Apidologie 38:606-611
32. Koeniger N, Wijayagunesekera HNP (1976) Time of drone flight in the three Asian honeybee species (Apis cerana, Apis florea, Apis dorsata). J Apic Res 15:67-71
33. Koeniger N, Koeniger G, Wongsiri S (1989) Mating and sperm transfer in Apis florea. Apidologie 20:413-418
34. Koeniger G, Koeniger N, Mardan M, Otis G, Wongsiri S (1991) Comparative anatomy of male genital organs in the genus Apis. Apidologie 22:539-552
35. Koeniger G, Koeniger N, Mardan M, Wongsiri S (1993) Variance in weight of sexuals and workers within and between 4 Apis species (Apis florea, Apis dorsata, Apis cerana and Apis mellifera). In: Proceedings of 1st international conference on Asian honey bees bee mites, Bangkok, Wicwas Press, Cheshire, pp 104-109
36. Koeniger G, Koeniger N, Tingek S (1994a) Mating flights, number of spermatozoa, sperm transfer and degree of polyandry in Apis koschevnikovi (Buttel-Reepen, 1906). Apidologie 25:224-238
37. Koeniger G, Koeniger N, Tingek S (1994b) Crossfostered drones of Apis cerana Fabricius, 1793 and Apis koschevnikovi v. Buttel-Reepen, 1906 fly at their species specific mating times. Insectes Soc 41:73-78
38. Koeniger N, Koeniger G, Tingek S, Kelitu A, Mardan M (1994c) Drones of Apis dorsata Fabricius, 1793 congregate under the canopy of tall emergent trees in Borneo. Apidologie 25:249-264
39. Koeniger N, Koeniger G, Mardan M (1994d) Mimicking a honeybee queen? Vespa affinis indosinensis Pérez 1919 hunts drones of Apis cerana F. 1793. Ethology 98:149-153
40. Koeniger G, Hänel H, Wissel M, Herth W (1996a) Cornual gland of the honey bee drone (Apis mellifera L.): structure and secretion. Apidologie 27:145-156
41. 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 27:353-360
42. Koeniger N, Koeniger G, Tingek S, Kelitu A (1996c) Interspecific rearing and acceptance of queens between Apis cerana Fabr. 1793 and Apis koschevnikovi Buttel-Reepen 1906. Apidologie 27:371-380
43. Koeniger N, Tingek S, Koeniger G, Gries M, Kelitu A (1998) Exploring the biodiversity of honeybees. Borneo 4:18-33
44. Koeniger G, Koeniger N, Tingek S, Kelitu A (2000) Mating flights and sperm transfer in the dwarf honey bee Apis andreniformis (Smith, 1858). Apidologie 31:301-311
45. Koeniger G, Koeniger N, Tingek S (2001) Diversity of the mating sign and its function in the genus Apis. In: Proceedings of the 7th international conference on tropical bees, Chiang Mai, pp 87-90
46. Koeniger N, Koeniger G, Gries M, Tingek S (2005) Drone competition at drone congregation areas in four Apis species. Apidologie 36:211-221
47. Koeniger N, Koeniger G, Tingek S (2010) Honey bee of Borneo, exploring the center of Apis diversity. Nat Hist Publ (Borneo), Kota Kinabalu, pp 53-60
48. Kraus FB, Neumann P, van Praagh J, Moritz RFA (2004) Sperm limitation and the evolution of polyandry in the honeybee (Apis mellifera L.). Behav Ecol Sociobiol 55:494-501
49. Kraus FB, Neumann P, Moritz RFA, Koeniger N, Tingek S (2005a) Using drones for estimating colony number by microsatellite DNA analyses of haploid males in Apis. Apidologie 36:223-229
50. Kraus FB, Neumann P, Moritz RFA (2005b) Genetic variance of mating frequency in the honeybee (Apis mellifera L.). Insectes Soc 52:1-5
51. Lap PV, Chinh PH, Chinh TX (1992) Some biological characteristics of A. cerana queen bees in Vietnam. In: Connor LJ, Rinderer TE, Sylvester HA, Wongsiri S (eds) Asian apiculture. Wicwac, Cheshire, pp 117-123
52. Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge
53. McEvoy M, Underwood BA (1988) The drone and species status of the Himalayan honey bee, Apis laboriosa (Hymenoptera: Apidae). J Kans Entomol Soc 61:246-249
54. Moors DL (2010) Functional-morphological study of the male reproductive system of honeybees. Dissertation. Katholieke Universiteit Leuven, pp 138-146
55. Moritz RFA (1993) Intracolonial relationship in the honey bee colony (Apis mellifera): molecular evidence and behavioural consequences. Verh Dtsch Zool Gesells 86:151-158
56. Moritz RFA, Fuchs S (1998) Organisation of honeybee colonies: characteristics and consequences of a superorganism concept. Apidologie 29:7-22
57. Moritz RFA, Southwick EE (1992) Bees as superorganisms - an evolutionary reality. Springer, Heidelberg
58. Moritz RFA, Kryger P, Koeniger G, Koeniger N, Estoup A, Tingek S (1995) High degree of polyandry in Apis dorsata queens detected by DNA microsatellite variability. Behav Ecol Sociobiol 37:357-363
59. Nagaraja N, Brockmann A (2009) Drone congregation areas of red dwarf honeybee, Apis florea. Nat Prec.: doi: 10101/npre. 2009. 3955.1
60. Nakamura J (1995) Brood cannibalism in colonies of Asian honeybee, A. cerana, as response to resource fluctuation. Tamagawa Univ Res Rev 1:33-48
61. Neumann P, Moritz RFA, van Praagh J (1999) Queen mating frequency in different types of honeybee mating apiaries. J Apic Res 38:11-18
62. Oldroyd BP, Wongsiri S (2006) Asian honey bees. Harvard University Press, Cambridge
63. Oldroyd BP, Smolenski AJ, Cornuet JM, Wongsiri S, Estoup A, Rinderer TE, Crozier RH (1996) Levels of polyandry and intracolonial genetic relationships in Apis dorsata (Hymenoptera: Apidae). Ann Entomol Soc Am 89:276-283
64. Oldroyd BP, Clifton MJ, Wongsiri S, Rinderer TE, Crozier RH (1997) Polyandry in the genus Apis, particularly Apis andreniformis. Behav Ecol Sociobiol 40:17-26
65. Oldroyd BP, Clifton MJ, Parker K, Wongsiri S, Rinderer TE, Crozier RH (1998) Evolution of mating behaviour in the genus Apis and an estimate of mating frequency in A. cerana (Hymenoptera: Apidae). Ann Entomol Soc Am 91:700-709
66. Otis GW, Hadisoesilo S (1996) Apis nigrocincta, a previously unrecognized honey bee species from Indonesia: Lessons in speciation. In: Proceedings of 3rd Asian apiculture association conference, Hanoi, pp 2-6
67. Otis GW, Patton K, Tingek S (1995) Piping by queens of Apis cerana Fabricius 1793 and Apis koschevnikovi von Buttel-Reepen 1906. Apidologie 26:61-65
68. Otis GW, Koeniger N, Rinderer TE, Hadisoesilo S, Yoshida T, Tingek S, Wongsiri S, Mardan MB (2001) Comparative mating flight times of Asian honey bees. In: Proceedings of 7th international conference on tropical bees, Chiang Mai, pp 137-141
69. Paar J, Oldroyd BP, Huettinger E, Kastberger G (2004) Levels of polyandry in Apis laboriosa Smith from Nepal. Insectes Soc 51:212-214
70. Palmer KA, Oldroyd BP (2000) Evolution of multiple mating in the genus Apis. Apidologie 33:553-561
71. Patinawin S, Wongsiri S (1993) Male genitalia of honey bees. In: Connor LJ, Rinderer TE, Sylvester HA, Wongsiri S (eds) Asian apiculture. Wicwas, Cheshire, pp 110-116
72. Pflugfelder J, Koeniger N, Svatos A, Crewe R (2004) Interspecific aggression among virgin queens (Apis mellifera, Apis cerana, Apis koschevnikovi and Apis florea) and evidence for a chemical releaser of queen fighting. In: Proceedings of 8th Asian apiculture association conference, Los Banos, p 362
73. Phiancharoen M, Wongsiri S, Koeniger N, Koeniger G (2004) Instrumental insemination of Apis mellifera queens with hetero- and conspecific spermatozoa results in different sperm survival. Apidologie 35:503-511
74. Plettner E, Otis GW, Wimalaratne PDC, Winston ML, Slessor KN, Pankiw T, Punchihewa RWK (1997) Species- and caste-determined mandibular gland signals in honeybees (Apis). J Chem Ecol 23:363-377
75. Punchihewa RWK (1992) Beobachtungen und Experimente zur Paarungsbiologie von Apis cerana indica in Sri Lanka. Thesis, Universität Frankfurt am Main [in German]
76. Punchihewa RWK (1994) Beekeeping for honey production in Sri Lanka. Sri Lanka Department of Agriculture
77. Punchihewa RWK, Koeniger N, Koeniger G (1990) Congregation of Apis cerana indica drones in the canopy of trees in Sri Lanka. Apidologie 21:201-208
78. Radloff SE, Hepburn HR, Koeniger G (2003) Comparison of flight design of Asian honeybee drones. Apidologie 34:1-6
79. Rinderer TE, Oldroyd BP, Wongsiri S, Sylvester HA, De Guzman LI, Potichot S, Sheppard WS, Buchman SL (1993) Time of drone flight in four honeybee species in southeastern Thailand. J Apic Res 32:27-33
80. Rinderer TE, Stelzer A, Oldroyd BP, Tingek S (1998) Levels of polyandry and intracolonial relationships in Apis koschevnikovi. J Apic Res 37:281-287
81. Roberts WC (1944) Multiple mating of queen bees proved by progeny and flight tests. Glean Bee Cult 72:255-259, 303
82. Rueppell O, Fondrk MK, Page RE (2005) Biodemographic analysis of male honey bee mortality. Aging Cell 4:13-19
83. Ruttner F (1956a) Zur Frage der Spermaübetragung bei der Bienenkönigin. Insectes Soc 3:351-359 [in German]
84. Ruttner F (1956b) The mating of the honeybee. Bee World 37:2-15
85. Ruttner F (1973) Drohnen von Apis cerana Fabr auf einem Drohnensammelplatz. Apidologie 4:41-44 [in German]
86. Ruttner F (1988) Biogeography and taxonomy of honeybees. Springer, Berlin
87. Ruttner F, Kaissling KE (1968) Über die interspezifische Wirkung des Sexuallockstoffes von Apis mellifica und Apis cerana. Zeit Vergl Physiol 59:362-370
88. Ruttner F, Koeniger G (1971) Die Füllung der Spermatheka der Bienenkönigin - aktive Einwanderung oder passiver Transport der Spermatozoen. Zeit Vergl Physiol 72:411-422 [in German]
89. Ruttner F, Maul V (1983) Experimental analysis of reproductive interspecies isolation of Apis mellifera L. and Apis cerana F. Apidologie 14:309-327
90. Ruttner F, Ruttner H (1965) Untersuchungen über die Flugaktivität und das Paarungsverhalten der Drohnen. II. Beobachtungen an Drohnensammelplätzen. Z Bienenforsch 8:1-9 [in German]
91. Ruttner F, Ruttner H (1966) Untersuchungen über die Flugaktivität und das Paarungsverhalten der Drohnen. IIl. Flugweite und Flugrichtung der Drohnen. Z Bienenforsch 8:332-254 [in German]
92. Ruttner F, Woyke J, Koeniger N (1972) Reproduction in Apis cerana. 1. Mating behaviour. J Apic Res 11:141-146
93. Ruttner F, Woyke J, Koeniger N (1973) Reproduction in Apis cerana. 2. Reproductive organs and natural insemination. J Apic Res 12:21-34
94. Sandhu AS, Singh S (1960) The biology and brood rearing activities of the little honeybee - Apis florea Fabricius. Indian Bee J 22:27-35
95. Schlüns H, Moritz RFA, Neumann P, Kryger P, Koeniger G (2005) Multiple nuptial flights, sperm transfer and the evolution of extreme polyandry in honeybee queens. Anim Behav 70:125-131
96. Seidl R (1980) Die Sehfelder und Ommatidien-Divergenzwinkel der drei kasten der Honigbien (A. mellifera). Verh Dtsch Zool Ges 367 [in German]
97. Sharma PJ (1960) Observations on the swarming and mating habits of the Indian honeybee. Bee World 41:121-125
98. Shearer DA, Boch R, Morse RA, Laigo FM (1970) Occurrence of 9-oxodec-trans-2-enoic acid in queens of Apis dorsata, Apis cerana and Apis mellifera. J Insect Physiol 16:1437-1441
99. Sherman PW, Seeley TD, Reeve HK (1988) Parasites, pathogens, and polyandry in social Hymenoptera. Am Nat 131:602-610
100. Snodgrass RE (1956) The anatomy of the honey bee. Cornell University Press, London
101. Taber S (1954) The frequency of multiple mating of queen honey bees. J Econ Entomol 47:995-998
102. Takahashi J, Hashim SB, Tingek S, Shimizua I, Yoshida T (2008) A scientific note on the levels of polyandry in the black dwarf honeybee Apis andreniformis from Malaysia. Apidologie 39:233-234
103. Tan NQ (2007) Biology of Apis dorsata in Vietnam. Apidologie 38:221-229
104. Tan NQ, Mardan MB, Thai PH, Chinh PH (1996) Some reproductive biology of Apis dorsata. In: Proceedings of 3rd Asian apiculture association conference, Hanoi, pp 15-22
105. Tan NQ, Mardan MB, Thai PH, Chinh PH (1999) Observations on multiple mating flights of Apis dorsata queens. Apidologie 30:339-346
106. Tarpy DR, Page RE (2001) The curious promiscuity of queen honey bees (Apis mellifera): evolutionary and behavioural mechanisms. Ann Zool Fennici 38:255-265
107. Tarpy DR, Nielsen R, Nielsen DI (2004) A scientific note on the revised estimates of effective paternity frequency in Apis. Insectes Soc 51:203-204
108. Triasko VV (1956a) Multiple matings of queen bees. Pchelovodstvo 34:29-31
109. Triasko VV (1956b) Polyandry in honey bees. XVI International beekeepers congress, Preliminary Science Meeting 233/56
110. Trivers RL, Hare H (1976) Haplodiploidy and the evolution of the social insects. Science 191:249-263
111. Underwood BA (1990) Time of drone flight of Apis laboriosa Smith, 1871 in Nepal. Apidologie 21:501-504
112. Vallet AM, Cole JA (1993) The perception of small objects by the drone honeybee. J Comp Physiol A 172:183-188
113. van Praagh JP, Ribi W, Wehrhan C, Wittmann D (1980) Drone bees fixate the queen with the dorso-frontal part of their compound eyes. J Comp Physiol 136:263-266
114. Verma LR (1973) An ionic basis for a possible mechanism of sperm survival in the spermatheca of the queen honey bee Apis mellifera. Comp Biochem Physiol 44:1325-1331
115. Verma LR (1991) Beekeeping in integrated mountain development. Oxford and IBH, New Delhi
116. von Berlepsch A (1873) Die Biene und ihre Zucht auf beweglichen Waben in Gegenden ohne Spätsommertracht, 3rd edn. J. Schneider, Mannheim [in German]
117. Wattanachaiyingcharoen W, Oldroyd BP, Wongsiri S, Palmer K, Paar S (2003) A scientific note on the mating frequency of Apis dorsata Fabricius. Apidologie 34:85-86
118. Weiss K (1962) Untersuchungen über die Drohnenbruterzeugung im bienenvolk. Arch Bienenkunde 39:1-7 [in German]
119. Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge
120. Woyke J (1960) Natural and artificial insemination of queen honeybees. Pszcz Zesz Nauk 4:183-275
121. Woyke J (1975) Natural and artificial insemination of Apis cerana in India. J Apic Res 14:153-159
122. Woyke J (1988) A mathematical model for the dynamics of spermatozoa entry into the spermathecae of instrumentally inseminated queen honeybees. J Apic Res 27:122-125
123. Woyke J (2001) Eversion of drone endophallus and the probable mating process in Apis dorsata. In: Proceedings of the 7th Asian apiculture association conference on tropical bees, Chiang Mai, pp 188-194
124. Woyke J (2008) Why the eversion of the endophallus of honey bee drone stops at the partly everted stage and significance of this. Apidologie 39:627-636
125. Woyke J, Ruttner F (1958) An anatomical study of the mating process in the honeybee. Bee World 39:3-18
126. Woyke J, Wilde J, Wilde M (2001) Apis dorsata drone flights, collection of semen from everted endophalli and instrumental insemination of queens. Apidologie 32:407-416
127. Wu Y, Kuang B (1986) A study of genus Micrapis (Apidae). Zool Res 7:99-102
128. Yoshida T (1995) Differences in mating flight times and drone congregation areas of native Apis cerana japonica and introduced Apis mellifera. Honeybee Sci 16:57-66
129. Yoshida T, Yamazaki M (1993) Difference in drone congregation areas of Apis mellifera and Apis cerana japonica as a reproductive isolation mechanism. In: Connor LK, Rinderer T, Sylvester A, Wongsiri S (eds) Asian apiculture. Wicwas, Cheshire, pp 99-103
130. Yoshida T, Saito J, Kajigaya N (1994) The mating flight times of native Apis cerana japonica Radoszkowski and introduced Apis mellifera L. in sympatric conditions. Apidologie 25:353-360