Social parasitism by honeybee workers (Apis mellifera capensis Esch.): Evidence for pheromonal resistance to host queen's signals

Behavioral Ecology and Sociobiology

Volumn 60, Issue 6, 2006, Pages 785-793

  Dietemann, Vincent ^a   Pflugfelder, Jochen ^b   Härtel, Stephan ^c   Neumann, Peter ^c,d,e   Crewe, Robin M ^a  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b GOETHE UNIVERSITY   (Germany)

^c MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^d RHODES UNIVERSITY   (South Africa)

^e YUNNAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

Apis mellifera capensis; Honeybee; Mandibular gland; Pheromonal competition; Social parasitism; Worker reproduction

Indexed keywords

HONEYBEE; PHEROMONE; QUEEN; REPRODUCTIVE STATUS; SOCIAL PARASITISM; WORKER CASTE;

APIS MELLIFERA; APIS MELLIFERA SCUTELLATA;

EID: 33748647412     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-006-0222-0     Document Type: Article

References (82)

1. Akre RD, Garnett WB, MacDonald JF, Greene A, Landolt P (1976) Behavior and colony development of Vespula pensylvanica and V. atropilosa (Hymenoptera: Vespidae). J Kans Entomol Soc 49:63-84
2. Allsopp MH (1993) Summarized overview of the capensis problem. S Afr Bee J 65:127-136
3. Allsopp MH, Crewe RM (1993) The Cape honeybee as a Trojan horse rather than the hordes of Jenghiz Khan. Am Bee J 133:121-123
4. Barbier J, Lederer E (1960) Structure chimique de la substance royale de la reine de l'abeille. C R Acad Sci Paris Série D 251:1131-1135
5. Baudry E, Kryger P, Allsopp M, Koeniger N, Vautrin D, Mougel F, Cornuet JM, Solignac M (2004) Whole-genome scan in thelytokous-laying workers of the Cape honeybee (Apis mellifera capensis): central fusion, reduced recombination rates and centromere mapping using half-tetrad analysis. Genetics 167:243-252
6. Beekman M, Wossler TC, Martin SJ, Ratnieks FLW (2002) Parasitic honeybee workers (Apis mellifera capensis) are not given preferential treatment by African guards (A. m. scutellata). Insectes Soc 49:216-220
7. Birmingham AL, Hoover SE, Winston ML, Ydenberg RC (2004) Drifting bumble bee (Hymenoptera: Apidae) workers in commercial greenhouses may be social parasites. Can J Zool 82:1842-1853
8. Breed MD, Diaz PH, Lucero KD (2004) Olfactory information processing in honeybee, Apis mellifera, nestmate recognition. Anim Behav 68:921-928
9. Callow RK, Johnston NC (1960) The chemical constitution and synthesis of queen substances of honeybees (A. mellifera L.). Bee World 41:152-153
10. Crewe RM (1982) Compositional variability: the key to the social signals produced by honeybee mandibular glands. In: Breed MD, Michener CD, Evan HE (eds) The biology of social insects. Westview, Boulder, CO, pp 318-322
11. Crewe RM (1984) Differences in behaviour and morphology between capensis and adansonii. S Afr Bee J 56:16-21
12. Crewe RM (1988) Natural history of honey-bee mandibular gland secretions: development of analytical techniques and the emergence of complexity. In: Needham GR, Page RE, Delfinado-Baker M, Bowman CE (eds) Africanized honeybees and bee mites. Ellis Horwood, Chichester, pp 149-158
13. D'Ettore P, Heinze J (2001) Sociobiology of slave-making ants. Acta Ethol 3:67-82
14. Dietemann V, Lubbe A, Crewe RM (2006) Human factors facilitating the spread of a parasitic honeybee in South Africa. J Econ Entomol 99:7-13
15. Härtel S, Neumann P, Raassen FS, Moritz RFA, Hepburn HR (2006a) Social parasitism by Cape honeybee workers in colonies of their own subspecies (Apis mellifera capensis Esch.). Insectes Soc (In press)
16. Härtel S, Neumann P, Kryger P, von der Heide C, Moltzer, G-J, Crewe RM, van Praagh JP, Moritz RFA (2006b) Infestation levels of Apis mellifera scutellata swarms by socially parasitic Cape honeybee workers (Apis mellifera capensis Esch.). Apidologie (In press) DOI: 10.1051/apido:2006012
17. Hemmling C, Koeniger N, Ruttner F (1979) Quantitative Bestimmung der 9-Oxodecensäure im Lebenszyklus der Kapbiene (Apis mellifera capensis Escholtz). Apidologie 10:227-240
18. Hepburn HR (1992) Pheromonal and ovarian development covary in Cape Honeybees, Apis mellifera capensis. Naturwissenschaften 79:523-524
19. Hepburn HR (1994) Reproductive cycling and hierarchical competition in Cape honeybees, Apis mellifera capensis Esch. Apidologie 25:38-48
20. Hepburn HR, Crewe RM (1991) Portrait of the Cape honeybee, Apis mellifera capensis. Apidologie 22:567-580
21. Hepburn HR, Radloff SE (1998) Honeybees of Africa. Springer, Berlin Heidelberg New York
22. Hillesheim E, Koeniger N, Moritz RFA (1989) Colony performance in honeybees (Apis mellifera capensis) depends on proportion of subordinate and dominant workers. Behav Ecol Sociobiol 24:291-296
23. Hölldobler B, Wilson EO (1990) The ants. Springer, Berlin Heidelberg New York
24. Hoover SER, Keeling CI, Winston ML, Slessor KN (2003) The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90:477-480
25. Hoover SER, Winston ML, Oldroyd BP (2005) Retinue attraction and ovary activation: response of wild type and anarchistic honeybees (Apis mellifera) to queen and brood pheromones. Behav Ecol Sociobiol 59:278-284
26. Hoover SER, Higo HA, Winston ML (2006) Worker honeybee ovary development seasonal variation and the influence of larval and adult nutrition. J Comp Physiol B 176:55-63
27. Jay SC (1972) Ovary development of worker honeybees when separated from worker brood by various methods. Can J Zool 50:661-664
28. Johannsmeier MF (1983) Experiences with the Cape bee in the Transvaal. S Afr Bee J 55:130-138
29. Katzav-Gozansky T, Soroker V, Hefetz A (2002) Honeybees Dufour's gland - idiosyncrasy of a new queen signal. Apidologie 33:525-537
30. Keeling CI, Slessor KN, Higo HA, Winston ML (2003) New components of the honey bee (Apis mellifera L.) queen retinue pheromone. Proc Natl Acad Sci USA 100:4486-4491
31. Keller L, Nonacs P (1993) The role of pheromone in social insects: queen control or queen signal? Anim Behav 45:787-794
32. Koeniger N, Würkner W (1992) Die Kap Honigbienen (Apis mellifera capensis) Natürliche Verbreitung und die Schwierigkeiten der Haltung unter unseren klimatischen Bedingungen. Die Biene 128:583-588
33. Kryger P (2001) The Capensis pseudo-clone, a social parasite of African honey bees. In: Proceedings of the 2001 Berlin Meeting of the European Section of IUSSI, p 208
34. Lenoir A, D'Ettorre P, Errard C (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573-599
35. Lopez-Vaamonde C, Koning JW, Brown RM, Jordan WC, Bourke AFG (2004) Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430:557-560
36. Lundie AE (1954) Laying workers produce worker bees. S Afr Bee J 29:10-11
37. Martin S, Wossler TC, Kryger P (2002a) Usurpation of Apis mellifera scutellata colonies by A. m. capensis workers. Apidologie 33:215-232
38. Martin SJ, Beekman M, Wossler TC, Ratnieks FLW (2002b) Parasitic Cape honeybee workers, Apis mellifera capensis evade policing. Nature 415:163-165
39. Michener CD (2000) The bees of the world. The Johns Hopkins University Press, Baltimore Maryland
40. Montague CE, Oldroyd BP (1998) The evolution of worker sterility in honey bees: an investigation into a behavioural mutant causing failure of worker policing. Evolution 52:1408-1415
41. Moritz RFA, Hillesheim E (1985) Inheritance of dominance in honeybees (Apis mellifera capensis Esch.). Behav Ecol Sociobiol 17:87-89
42. Moritz RFA, Haberl M (1994) Lack of meiotic recombination in thelytokous parthenogenesis of laying workers of Apis mellifera capensis (the Cape honeybee). Heredity 73:98-102
43. Moritz RFA, Kryger P, Allsopp MH (1999) Lack of worker policing in the Cape honey bee (Apis mellifera capensis) Behaviour 136:1079-1092
44. Moritz RFA, Simon UE, Crewe RM (2000) Pheromonal contest between honeybee workers. Naturwissenschaften 87:395-397
45. Moritz RFA, Lattorff HMG, Crewe RM (2004) Honeybee workers (Apis mellifera capensis) compete for producing queen-like pheromone signals. Proc R Soc Lond B Biol Sci 271(Suppl 3):98-100
46. Nanork P, Paar J, Chapman NC, Wongsiri S, Oldroyd BP (2005) Asian honeybees parasitize the future dead. Nature 437:829
47. Naumann K, Winston ML, Slessor K, Prestwich GD, Webster FX (1991) Production and transmission of honey bee queen (Apis mellifera L.) mandibular gland pheromone. Behav Ecol Sociobiol 29:321-332
48. Neumann P, Hepburn HR (2002) Behavioural basis for social parasitism of Cape honeybees (Apis mellifera capensis Esch.). Apidologie 33:165-192
49. Neumann P, Moritz RFA (2002) The Cape honeybee phenomenon: the sympatric evolution of a social parasite in real-time. Behav Ecol Sociobiol 52:271-281
50. Neumann P, Radloff SE, Hepburn HR (2002) Parasitic Cape bees in the northern regions of South Africa: source of the founder population. S Afr J Sci 98:404-406
51. Oldroyd BP, Smolenski AJ, Cornuet JM, Crozier RH (1994) Anarchy in the beehive. Nature 371:749
52. Onions GW (1912) South African "fertile-worker bees". S Afr Agric J 1:720-728
53. Pankiw T, Winston ML, Plettner E, Slessor KN, Pettis JS, Taylor OR (1996) Mandibular gland components of European and Africanized honey bee queens. J Chem Ecol 22:605-615
54. Pirk CWW, Neumann P, Ratnieks FLW (2003) Cape honeybees, Apis mellifera capensis, police worker-laid eggs despite the absence of relatedness benefits. Behav Ecol 14:347-352
55. Pirk CWW, Neumann P, Hepburn HR, Moritz RFA, Tautz J (2004) Egg viability and worker policing in honeybees. Proc Natl Acad Sci USA 101:8649-8651
56. Plettner E, Slessor KN, Winston ML, Robinson GE, Page RE (1993) Mandibular gland components and ovarian development as measures of caste differentiation in the honey bee (Apis mellifera L.). J Insect Physiol 39:235-240
57. Ratnieks FL (1993) Egg-laying, egg-removal, and ovary development by workers in queenright honeybee colonies. Behav Ecol Sociobiol 32:191-198
58. Ratnieks FLW, Visscher PK (1989) Worker policing in the honeybee. Nature 342:796-797
59. Ruttner F (1980) Königinnenzucht. Apimondia, Bukarest
60. Ruttner F, Koeniger N (1976) Queen substance bei eierlegenden Arbeiterinnen der Honigbiene (Apis mellifera L.). Naturwissenschaften 9:434-435
61. Sakagami SF (1958) The false queen: fourth adjustive response in dequeened honeybee colonies. Behaviour 13:280-296
62. Sasaki T, Tsuji K (2003) Behavioral property of the unusual large workers in the ant, Pristomyrmex pungens. J Ethol 21:145-151
63. Schäfer MO, Dietemann V, Pirk CWW, Neumann P, Crewe RM, Hepburn HR, Tautz J, Crailsheim K (2006) Pollen consumption and worker reproduction in Cape honeybees (Apis mellifera capensis Esch.) J Comp Physiol (In press) DOI 10.1007/s00359-006-0112-y
64. Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton, NJ
65. Simon UE, Moritz RFA, Crewe RM (2001) The ontogenetic pattern of mandibular gland components in queenless worker bees (Apis mellifera capensis Esch.). J Insect Physiol 47:735-738
66. Simon U, Moritz RFA, Crewe RM (2005) Reproductive dominance among honeybee workers in experimental groups of Apis mellifera capensis. Apidologie 36:413-419
67. Slessor KN, Kaminski LA, Ki GGS, Borden JH, Winston ML (1988) Semiochemical basis of the retinue response to queen honey bees. Nature 332:354-356
68. Slessor KN, Kaminski LA, King GGS, Winston ML (1990) Semiochemicals of the honey bee queen mandibular glands. J Chem Ecol 16:851-860
69. Slessor KN, Winston ML, Le Conte Y (2005) Pheromone communication in the honeybee. J Chem Ecol 31:2731-2745
70. Tribe GD (1981) Cape honeybee behaviour. S Afr Bee J 53:10-12
71. Tsuji K (1995) Reproductive conflicts and levels of selection in the parthenogenetic ant, Pristomyrmex pungens: contextual analysis and partitioning of covariance. Am Nat 146:586-607
72. van der Blom J (1991) Social regulation of egg-laying by queenless honeybee workers (Apis mellifera L.). Behav Ecol Sociobiol 29:341-346
73. Velthuis HHW, van der Kerk A (1988) Age, environment, and genes in relation to the mandibular gland secretion of pure and hybrid Apis mellifera capensis worker bees. In: Needham GR, Page RE, Delfinado-Baker M, Bowman CE (eds) Africanized honeybees and bee mites. Ellis Horwood, Chichester, pp 80-86
74. Velthuis HHW, Ruttner F, Crewe RM (1990) Differentiation in reproductive physiology and behaviour during the development of laying worker honeybees. In: Engels W (ed) Social insects. Springer, Berlin Heidelberg New York, pp 231-243
75. Vierling G, Renner M (1977) Secretion of tergite glands and attractiveness of honey bee queen. Behav Ecol Sociobiol 2:185-200
76. Visscher PK (1989) A quantitative study of worker reproduction in honey bee colonies. Behav Ecol Sociobiol 25:247-254
77. Visscher PK (1996) Reproductive conflict in honey bees: a stalemate of worker egg-laying and policing. Behav Ecol Sociobiol 39:237-244
78. Visscher PK, Dukas R (1995) Honey bees recognise development of nestmates' ovaries. Anim Behav 49:542-544
79. Wilson EO (1971) The insect societies. Cambridge, Harvard University Press
80. Winston ML, Slessor KN (1998) Honey bee primer pheromones and colony organization: gaps in our knowledge. Apidologie 29:81-95
81. Wossler TC, Crewe RM (1999) Honey bee tergal gland secretion affects ovarian development in caged workers. Apidologie 30:311-320
82. Woyke J (1995) Invasion of Capensis bee. In: Magnuson P (ed) Proceedings of the first international electronic conference on the Cape bee problem in South Africa. Plant Protection Research Institute, Pretoria, South Africa, p 35