, 93:315 | Cite as

Gigantism in honeybees: Apis cerana queens reared in mixed-species colonies

  • Ken Tan
  • H. R. HepburnEmail author
  • Shaoyu He
  • S. E. Radloff
  • P. Neumann
  • Xiang Fang
Original Article


The development of animals depends on both genetic and environmental effects to a varying extent. Their relative influences can be evaluated in the social insects by raising the intracolonial diversity to an extreme in nests consisting of workers from more than one species. In this study, we studied the effects of mixed honeybee colonies of Apis mellifera and Apis cerana on the rearing of grafted queen larvae of A. cerana. A. mellifera sealed worker brood was introduced into A. cerana colonies and on emergence, the adults were accepted. Then, A. cerana larvae were grafted for queen rearing into two of these mixed-species colonies. Similarly, A. cerana larvae and A. mellifera larvae were also grafted conspecifically as controls. The success rate of A. cerana queen rearing in the test colonies was 64.5%, surpassing all previous attempts at interspecific queen rearing. After emergence, all virgin queens obtained from the three groups (N=90) were measured morphometrically. The A. cerana queens from the mixed-species colonies differed significantly in size and pigmentation from the A. cerana control queens and closely approximated the A. mellifera queens. It is inferred that these changes in the A. cerana queens reared in the mixed-species colonies can be attributed to feeding by heterospecific nurse bees and/or chemical differences in royal jelly. Our data show a strong impact of environment on the development of queens. The results further suggest that in honeybees the cues for brood recognition can be learned by heterospecific workers after eclosion, thereby providing a novel analogy to slave making in ants.


Linear Discriminant Analysis Royal Jelly Virgin Queen Host Coloni Queen Rear 
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.



We are grateful to two anonymous referees for their constructive comments. Financial support was granted by the Xishuangbanna Tropical Botanical Garden, Chinese Academy of Science and the Yunnan agricultural University of China to TK and by the DFG to PN.


  1. Atwal AS, Sharma OP (1967) The introduction of Apis mellifera queens into Apis indica colonies and the associated behavior of the two species. XXI International Beekeeping Congress, Preliminary Science Meeting, Summary Paper 70–77.Google Scholar
  2. Adlakha RL, Sharma OP (1971) Interspecific introduction of queens (Apis mellifera queens into A. indica nuclei). Proceedings of the 23rd International Apiculture Congress, Moscow. Apimondia 402.Google Scholar
  3. Ayasse M, Paxton RJ (2002) Brood protection in social insects. In: Hilker M, Meiners T (eds) Chemoecology of insect eggs and egg deposition. Blackwell, Oxford, pp 117–148Google Scholar
  4. Breed MD, Perry S, Bjostad LB (2004) Testing the blank slate hypothesis: why honey bee colonies accept young bees. Insectes Soc 51:12–16CrossRefGoogle Scholar
  5. Dhaliwal GS, Atwal AS (1970) Interspecific relations between Apis cerana indica and Apis mellifera. J Apic Res 9:53–59Google Scholar
  6. Hölldobler B, Wilson EO (1990) The Ants. Harvard University Press, CambridgeGoogle Scholar
  7. Inoue A (1962) Preliminary report on the rearing of Japanese honeybee queens in colonies of the European honeybee. Indian Bee J 24:73–74Google Scholar
  8. Johnson RA, Wichern DW (1998) Applied multivariate statistical analysis, Fourth Edition, Prentice-Hall, Upper Saddle River, New JerseyGoogle Scholar
  9. Kuwabara M (1947) Über die Regulation im weisellosen Volke der Honigbiene, besonders die Bestimmung des neuen Weisels. J Fac Sci Hokkaido Univ Ser 6, 9:359–381Google Scholar
  10. Laloi D, Gallois M, Roger B Pham-Delegue MH (2001) Changes with age in olfactory conditioning performance of worker honey bees (Apis mellifera). Apidologie 32:231–242CrossRefGoogle Scholar
  11. Matsuka M, Tsurata T, Sasaki M (1995) Temperature as a causative factor of the seasonal colour dimorphism in Apis cerana japonica. In: Kevan PG (ed) The Asiatic hive bee: apiculture, biology, and role in sustainable development in tropical and subtropical AsiaGoogle Scholar
  12. Meixner M (1994) Analyse polymorpher Subspezies von A. mellifera L.: Morphometrische und molekulare Untersuchungen an den europäischen Rassen A. mellifera carnica und ligustica und den afrikanischen Rassen A. mellifera monticola und scutellata. Ph.D. thesis, Fachbereich Biologie der J. W. Goethe-Universität, Frankfurt am Main, GermanyGoogle Scholar
  13. Oku N, Ono M (1990) Preliminary attempts to rear larvae of the Japanese honeybee, Apis cerana japonica, in an Apis mellifera colony and in the laboratory using A. mellifera royal jelly. Honeybee Sci 3:121–124 (in Japanese)Google Scholar
  14. Oschmann H (1965) Can Apis mellifica bees rear brood of A. cerana? Die Biene Giessen 101:150–151 (in German)Google Scholar
  15. Pham-Delegue MH, Trouiller J, Caillaud CM, Roger B, Masson C (1993) Effect of queen pheromone on worker bees of different ages: behavioural and electrophysiological responses. Apidologie 24:267–281CrossRefGoogle Scholar
  16. Potichot S, Wongsiri S, Dietz A (1993) Attempts in queen rearing of Apis cerana larvae in Apis mellifera colonies and Apis mellifera larvae in Apis cerana colonies. In Connor LJ, Rinderer TE, Sylvester HA, Wongsiri S (eds) Asian apiculture, Wicwas, Cheshire, Connecticut, pp 128–133Google Scholar
  17. Ribbands CR (1953) The behaviour and social life of honeybees. Bee Research Association, LondonGoogle Scholar
  18. Ruttner F (1988) Biogeography and taxonomy of honeybees. Springer, Berlin Heidelberg New YorkGoogle Scholar
  19. Ruttner F, Tassencourt L, Louveaux J (1978) Biometrical-statistical analysis of the geographic variability of Apis mellifera. Apidologie 9:363–381CrossRefGoogle Scholar
  20. Su S, Albert S, Chen S, Zhong B (2005) Molecular cloning and analysis of four cDNAs from the heads of Apis cerana cerana nurse honeybees coding for major royal jelly proteins. Apidologie 36:389–401CrossRefGoogle Scholar
  21. Takenaka T, Takenaka Y (1996) Royal jelly from Apis cerana and Apis mellifera. Biosci Biotechnol Biochem 60:518–520CrossRefGoogle Scholar
  22. Tsurata T, Matsuka M, Sasaki M (1989) Temperature as a causative factor in the seasonal colour dimorphism of Apis cerana japonica workers. Apidologie 20:149–155CrossRefGoogle Scholar
  23. Whiffler LA, Drusedau MUH, Crewe RN, Hepburn HR (1988) Defensive behaviour and the division of labour in the African honeybee (Apis mellifera scutellata). J Comp Physiol A 163:401–411CrossRefGoogle Scholar
  24. Yang GH (2001) Chinese honeybee (Apis cerana). Editorial House of China Agricultural Science and Technology, Beijing (in Chinese)Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Ken Tan
    • 1
    • 2
  • H. R. Hepburn
    • 2
    • 3
    Email author
  • Shaoyu He
    • 2
  • S. E. Radloff
    • 4
  • P. Neumann
    • 2
    • 3
    • 5
  • Xiang Fang
    • 2
  1. 1.Xishuangbanna Tropical Botanical GardenChinese Academy of ScienceYunnan ProvincePeople’s Republic of China
  2. 2.Eastern Bee research Institute of Yunnan Agricultural UniversityYunnan ProvincePeople’s Republic of China
  3. 3.Department of Zoology and EntomologyRhodes UniversityGrahamstown 6140South Africa
  4. 4.Department of StatisticsRhodes UniversityGrahamstown 6140South Africa
  5. 5.Institut für Zoologie, Molekulare ÖkologieMartin-Luther-Universität Halle-WittenbergHalle (Saale)Germany

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