Advertisement

Apidologie

pp 1–8 | Cite as

Apis florea workers show a prolonged period of nursing behavior

  • Hemalatha Bhagavan
  • Axel BrockmannEmail author
Original article

Abstract

Studies on behavioral maturation and division of labor in open-nesting honey bee species are scarce as the bee curtain inhibits direct examination of intranidal behaviors. We observed and studied nursing behavior in Apis florea by attaching a foreign comb with open brood to a host colony. Several of the workers that explored the attached comb visited the cells with brood more often and spent more time in cells compared to empty cells. Workers seen inspecting and feeding the brood had well-developed hypopharyngeal glands compared to foragers of their own colony indicating that they are nurses performing nursing behavior. Further, introducing marked 1-day-old workers into the host colony and repeatedly attaching combs with open brood allowed us to estimate the age range of nursing behavior. In our experiments, A. florea workers started to perform significant nursing behavior 8 days after eclosion and continued to show nursing behavior until the age of 28 days, the end of our observation period. Thus, nursing behavior in A. florea appears to be substantially extended relative to A. mellifera.

Keywords

Honey bee Hypopharyngeal gland Behavioral maturation Division of labor 

Notes

Acknowledgements

We would like to thank Hanumantha Raju for finding and collecting A. florea colonies as well as E.A. George help with statistical assistance. P.L. Kohl, S. Unnikrishnan, and A. Young and the reviewers for their helpful suggestions to improve the manuscript.

Authors’ contribution

HB and AB designed the study. HB performed and analyzed the experiments. HB and AB wrote the manuscript.

Funding information

The research was supported by NCBS institutional funds to AB (12P4167).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Anderson, C., Theraulaz, G., Deneubourg, J.-L. (2002) Self-assemblages in insect societies. Insectes Soc.,  https://doi.org/10.1007/s00040-002-8286-y
  2. Bhagavan, H., Muthmann, O., Brockmann, A. (2016) Structural and temporal dynamics of the bee curtain in the open-nesting honey bee species, Apis florea. Apidologie,  https://doi.org/10.1007/s13592-016-0428-8
  3. Brouwers, E V M. (1982) Measurement of hypopharyngeal gland activity in the honey bee. J. Apic. Res.,  https://doi.org/10.1080/00218839.1982.11100541
  4. Brouwers, E.V.M., Ebert, R. Beetsma, J., (1987) Behavioural and physiological aspects of nurse bees in relation to the composition of larval food during caste differentiation in the honeybee. J. Apic. Res.,  https://doi.org/10.1080/00218839.1987.11100729
  5. Calderone, N.W., Page, R.E. (1988) Genotypic variability in age polyethism and task specialization in the honey bee, Apis mellifera (Hymenoptera: Apidae). Behav. Ecol. Sociobiol.,  https://doi.org/10.1007/BF00395694
  6. Dyer, F.C., Seeley, T.D. (1991) Nesting-behavior and the evolution of worker tempo in 4 honeybee species. Ecology 72 (1), 156–170CrossRefGoogle Scholar
  7. Farris, S.M. (2016) Insect societies and the social brain. Curr. Opin. Insect Sci.,  https://doi.org/10.1016/j.cois.2016.01.010
  8. Fischman, B.J., Woodard S.H., Robinson, G E. (2011) Molecular evolutionary analyses of insect societies. PNAS,  https://doi.org/10.1073/pnas.1100301108
  9. Free, J. B. (1981) Biology and behaviour of the honey bee Apis florea, and possibilities for beekeeping. Bee World,  https://doi.org/10.1080/0005772X.1981.11097817
  10. Friard, O. and Gamba, M. (2016), BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol., 7: 1325–1330CrossRefGoogle Scholar
  11. Frumhoff, P.C., Baker, J. (1988) A genetic component to division of labour within honey bee colonies. Nature,  https://doi.org/10.1038/333358a0
  12. Fukunda, H., Sakagami, S.F. (1968) Worker brood survival in honeybees. Res. Pop. Ecol. 10: 31–39CrossRefGoogle Scholar
  13. Halling, L.A., B.P. Oldroyd, W. Wattanachaiyingcharoen, A.B. Barron, P. Nanork, S. Wongsiri(2001) Worker policing in the bee Apis florea. Behav. Ecol. Sociobiol. 49: 509–513CrossRefGoogle Scholar
  14. Haydak, M.H., (1963) Age of Nurse Bees and Brood Rearing. J. Apic. Res.,  https://doi.org/10.1080/00218839.1963.11100067
  15. Hepburn, H. R., Radloff, S.E. (2011) Honeybees of Asia. Springer-Verlag, Berlin HeidelbergCrossRefGoogle Scholar
  16. Hrassnigg, N., Crailsheim, K. (1998) Adaptation of hypopharyngeal gland development to the brood status of honeybee (Apis mellifera L.) colonies. J. Insect Physiol. 44 (10), 929–939CrossRefGoogle Scholar
  17. Huang, Z.Y., Otis, G.W. (1991a) Nonrandom visitation of brood cells by worker honey bees (Hymenoptera: Apidae). J. Insect Behav. 4 (2), 177–184CrossRefGoogle Scholar
  18. Huang, Z.Y., Otis, G.W. (1991b) Inspection and feeding of larvae by worker honey bees (Hymenoptera, Apidae)—effect of starvation and food quantity. J. Insect Behav. 4 (3), 305–317CrossRefGoogle Scholar
  19. Huang, Z.Y., Robinson, G E., Borst, D. W. (1994) Physiological correlates of division of labor among similarly aged honey bees. J. Comp. Physiol.,  https://doi.org/10.1007/BF00192722
  20. Johnson, B.R., Frost, E. (2012) Individual level patterns of division of labor in honey bees highlight flexibility in colony-level developmental mechanisms. Behav. Ecol. Sociobiol.,  https://doi.org/10.1007/s00265-012-1341-4
  21. Kolmes, SA. (1985) A quantitative study of the division of labor among worker honey bees. Z. Tierpsychol. 68 (4), 287–302CrossRefGoogle Scholar
  22. Lindauer, M. (1952) Ein Beitrag zur Frage der Arbeitsteilung im Bienenstaat. Z. Vergl. Physiol. S. 299–345.Google Scholar
  23. Nowogrodzki, R. (1984) Division of labour in the honey bee colony: A review, Bee World,  https://doi.org/10.1080/0005772X.1984.11098788
  24. Oldroyd B.P., Wongsiri S. (2006) Asian Honey Bees: Biology, Conservation, and Human Interactions. Harvard University Press, Boston MassGoogle Scholar
  25. Otis, G.W., Mardan, M., McGee, K. (1990) Age polytheism in Apis dorsata. In social insects and the environment. Proc. of the 11th Congress of IUSSI. Bangalore, pp. 378Google Scholar
  26. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., and R Core Team (2018). nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-137, https://www.CRAN.R-project.org/package=nlme
  27. Ribbands, C.R. (1952) Division of labour in the honeybee community. Proc. R. Soc. B.,  https://doi.org/10.1098/rspb.1952.0041
  28. Robinson G. E., Fernald R. D, Clayton D.F. (2008) Genes and social behavior. Science,  https://doi.org/10.1126/science.1159277
  29. Schmickl, T., Crailsheim, K. (2001) Inner nest homeostasis in a changing environment with special emphasis on honey bee brood nursing and pollen supply. Apidologie  https://doi.org/10.1051/apido:2004019
  30. Schmickl, T., Blaschon, B., Gurmann, B., Crailsheim, K. (2003) Collective and individual nursing investment in the queen and in young and old honeybee larvae during foraging and non-foraging periods. Insect. Soc. 50, 174–184CrossRefGoogle Scholar
  31. Seeley, T.D. (1982) Adaptive significance of the age polyethism schedule in honey bee colonies. Behav. Ecol. Sociobiol,  https://doi.org/10.1007/BF00299306
  32. Seeley, T.D. (1985) Honey bee ecology. A study of adaptation in social life. Princeton University Press; USA. ISBN 0–691-08391. pp 31–36Google Scholar
  33. Seeley, T.. (1995) The wisdom of the hive: the social physiology of honey bee colonies Harvard University Press. 1996Google Scholar
  34. Seeley, T.D., Morse, R.A. (1976) The nest of honey bee (Apis mellifera L.) Insectes Soc.,  https://doi.org/10.1007/BF02223477
  35. Sen Sarma, M., Whitfield, C.W., Robinson, G.E. (2007) Species differences in brain gene expression profiles associated with adult behavioral maturation in honey bees. BMC Genomics,  https://doi.org/10.1186/1471-2164-8-202
  36. Smodiš Škerl, Maja I., Gregorc, A. (2015) Characteristics of hypopharyngeal glands in honey bees (Apis Mellifera Carnica) from a nurse colony. Slov. Vet. Res. 52 (2), 67–74Google Scholar
  37. Winston, Mark L., and Elizabeth Neilson Punnett. (1982) Factors determining temporal division of labor in honeybees. Can. J. Zool.,  https://doi.org/10.1139/z82-372
  38. Wongvilas, S., J.S. Higgs, M. Beekman, W. Wattanachaiyingcharoen, S. Deowanish et al., 2010 Lack of inter-specific parasitism between the dwarf honeybees Apis andreniformis and Apis florea. Behavioral Ecology and Sociobiology 64:1165–1170.CrossRefGoogle Scholar

Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.National Centre for Biological SciencesTata Institute of Fundamental ResearchBangaloreIndia
  2. 2.Manipal UniversityManipalIndia

Personalised recommendations