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Individual versus social pathway to honeybee worker reproduction (Apis mellifera): pollen or jelly as protein source for oogenesis?

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Abstract

Honeybee workers, Apis mellifera, can reproduce in queenless colonies. The production of queen-like pheromones may be associated with their reproductive activity and induce nestmates to respond by feeding them. Such frequent trophallaxis could supply their protein needs for oogenesis, constituting a social pathway to worker reproduction. However, some individuals can develop ovaries without producing queen pheromones. The consumption of protein-rich pollen could be an alternative solitary pathway for them to satisfy this dietary requirement. In order to investigate the way in which workers obtain proteins for oogenesis, we created orphaned worker groups and determined ovarian and pheromonal development in relation to pollen consumption of selected workers. Individuals that did not consume pollen had significantly more developed ovaries and produced significantly more queen mandibular pheromone than workers that fed directly on pollen. Our results suggest that workers producing queen-like secretions are fed trophallactically. However, reproductive workers that lacked queen pheromones had consumed little or no pollen, suggesting that they also obtained trophallaxis. Although pollen consumption might contribute to sustaining oogenesis, it does not appear to be sufficient. Trophallaxis as a means of obtaining proteins seems to be necessary to attain reproductive status in queenless honeybee colonies.

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References

  • Allen MD (1955) Observations of honeybees attending their queen. Brit J Anim Behav 3:66–69

    Article  Google Scholar 

  • Allen MD (1960) The honeybee queen and her attendants. Anim Behav 8:201–208

    Article  Google Scholar 

  • Anderson RH (1963) The laying worker in the Cape honeybee Apis mellifera capensis. J Apic Res 2:85–92

    Google Scholar 

  • Barbier M, Lederer E (1960) Structure chimique de la ‘substance royale’ de la reine d’abeille (Apis mellifica). C R Acad Sci (Paris) 250:4467–4469

    CAS  Google Scholar 

  • Barker RJ, Lehner Y (1972) A look at honey bee gut functions. Am Bee J 112:336–338

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bitondi MMG, Simões ZLP (1996) The relationship between level of pollen in the diet and juvenile hormone titres in africanized Apis mellifera workers. J Apic Res 35:27–36

    CAS  Google Scholar 

  • Boch R, Shearer DA, Shuel RW (1979) Octanoic and other volatile acids in the mandibular gland of the honeybee and in royal jelly. J Apic Res 18:250–253

    CAS  Google Scholar 

  • Bourke AFG (1988) Worker reproduction in the higher eusocial Hymenoptera. Q Rev Biol 63:291–311

    Article  Google Scholar 

  • Buttel-Reepen H v (1900) Sind die Bienen Reflexmaschinen? Leipzig

  • Callow RK, Johnston NC, Simpson J (1959) 10-hydroxy-delta 2-decenoic acid in the honeybee (Apis mellifera). Experientia 15:421–422

    Article  PubMed  CAS  Google Scholar 

  • Choe J (1988) Worker reproduction and social evolution in ants (Hymenoptera: Formicidae). In: Trager JC (ed) Advances in myrmecology. Brill EJ, Leiden, pp 163–187

    Google Scholar 

  • Crailsheim K (1990) The protein balance of the honey bee worker. Apidologie 21:417–429

    Article  CAS  Google Scholar 

  • Crailsheim K (1991) Interadult feeding of jelly in honeybee (Apis mellifera L.) colonies. J Comp Physiol B 161:55–60

    Article  Google Scholar 

  • Crailsheim K, Schneider LHW, Hrassnigg N, Bühlmann G, Brosch U, Gmeinbauer R, Schöffmann B (1992) Pollen consumption and utilization in worker honey bees (Apis mellifera carnica): dependence on individual age and function. J Insect Physiol 38:409–419

    Article  Google Scholar 

  • Cremonez TM, De Jong D, Bitondi MMG (1998) Quantification of hemolymph proteins as a fast method for testing protein diets of honey bees (Hymenoptera: Apidae). J Econ Entomol 91:1284–1289

    CAS  Google Scholar 

  • 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 Limited, England, pp 149–158

    Google Scholar 

  • Crewe RM, Velthuis HHW (1980) False queens: a consequence of mandibular gland signals in worker honeybees. Naturwissenschaften 67:467–469

    Article  Google Scholar 

  • Free JB, Ferguson AW, Simpkins JR (1992) The behaviour of queen honeybees and their attendants. Physiol Entomol 17:43–55

    Article  Google Scholar 

  • Greeff JM (1996) Thelytokous versus arrhenotokous worker reproduction in the Cape honeybee and other eusocial Hymenoptera. Hereditas 124:99–103

    Article  Google Scholar 

  • Grogan DE, Hunt JH (1979) Pollen proteases: their potential role in insect digestion. Insect Biochem 9:309–313

    Article  CAS  Google Scholar 

  • Happ GM (1984) Major life systems. In: Evans HE (eds) Insect biology. Addison-Wesley publishing, Reading, MA, pp 70–92

    Google Scholar 

  • Haydak MH (1970) Honey bee nutrition. Ann Rev Entomol 15:143–156

    Article  Google Scholar 

  • Hemmling C, Koeniger N, Ruttner F (1979) Quantitative Bestimmung der 9-Oxodecensäure im Lebenszyklus der Kapbiene (Apis mellifera capensis Escholtz). Apidologie 10:227–240

    Article  CAS  Google Scholar 

  • Hepburn HR (1992) Pheromonal and ovarian development covary in Cape Honeybees, Apis mellifera capensis. Naturwissenschaften 79:523–524

    Article  Google Scholar 

  • Hepburn HR (1994) Reproductive cycling and hierarchical competition in Cape honeybees, Apis mellifera capensis Esch. Apidologie 25:38–48

    Article  Google Scholar 

  • Hepburn HR, Allsopp MH (1994) Reproductive conflict between honeybees: usurpation of Apis mellifera scutellata colonies by Apis mellifera capensis. S Afr J Sci 90:247–249

    Google Scholar 

  • Hepburn HR, Neumann P, Radloff SE (2004) Genetic variation in natural honeybee populations, Apis mellifera capensis Esch. Naturwissenschaften 91:447–450

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hoover SER, Keeling CI, Winston ML, Slessor KN (2003) The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90:477–480

    Article  PubMed  CAS  Google Scholar 

  • Howe SR, Dimick PS, Benton AW (1985) Composition of freshly harvested and commercial royal jelly. J Apic Res 24:52–61

    CAS  Google Scholar 

  • Klungness LM, Peng YS (1984a) A histochemical study of pollen digestion in the alimentary canal of honeybees (Apis mellifera L). J Insect Physiol 30:511–521

    Article  Google Scholar 

  • Klungness LM, Peng YS (1984b) Scanning electron microscope observation of pollen food bolus in the alimentary canal of honeybees. Can J Zool 62:1316–1319

    Article  Google Scholar 

  • Lin H, Winston ML (1998) The role of nutrition and temperature in the ovarian development of the worker honey bee (Apis mellifera). Can Entomol 130:883–891

    Article  Google Scholar 

  • Loidl A, Crailsheim K (2001) Free fatty acids from pollen and triolein in the honeybee (Apis mellifera carnica Pollmann) midgut. J Comp Physiol B 171:313–319

    Article  PubMed  CAS  Google Scholar 

  • Moritz B, Crailsheim K (1987) Physiology of protein digestion in the midgut of the honeybee (Apis mellifera L.). J Insect Physiol 33:923–931

    Article  CAS  Google Scholar 

  • Moritz RFA, Hillesheim E (1985) Inheritance of dominance in honeybees (Apis mellifera capensis). Behav Ecol Sociobiol 17:87–89

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Moritz RFA, Kryger P, Allsopp M (1996) Competition for royalty in bees. Nature 384:522

    Article  CAS  Google Scholar 

  • Moritz RFA, Simon UE, Crewe RM (2000) Pheromonal contest between honeybee workers. Naturwissenschaften 87:395–397

    Article  PubMed  CAS  Google Scholar 

  • Moritz RFA, Lattorff HMG, Crewe RM (2004) Honeybee workers (Apis mellifera capensis) compete for producing queen-like pheromone signals. Biol Lett Proc R Soc Lond (Suppl) 271:98–100

    Article  CAS  Google Scholar 

  • Neumann P, Hepburn HR (2002) Behavioural basis for social parasitism of Cape honeybees (Apis mellifera capensis Esch.). Apidologie 33:165–192

    Article  Google Scholar 

  • Onions GW (1909) Bees: workers and queens from eggs laid by workers. Agric J Cape Good Hope 35:527

    Google Scholar 

  • Pankiw T, Winston ML, Plettner E, Slessor KN (1996) Mandibular gland pheromone components of European and Africanized honey bee queens (Apis mellifera L.). J Chem Ecol 22:605–615

    Article  CAS  Google Scholar 

  • Peng YS, Nasr ME, Marston JM (1986) Release of alfalfa, Medicago sativa, pollen cytoplasm in the gut of the honey bee, Apis mellifera (Hymenoptera: Apidae). Ann Entomol Soc Am 79:804–807

    Google Scholar 

  • Pettis JS, Westcott LC, Winston ML (1998) Balling behaviour in the honey bee in response to exogenous queen mandibular gland pheromone. J Apic Res 37:125–131

    CAS  Google Scholar 

  • Ribbands CR (1953) The behaviour and social life of honeybees. Bee Research Association, London

    Google Scholar 

  • Robinson GE (1999) Integrative animal behaviour and sociogenomics. TREE 14:202–205

    PubMed  Google Scholar 

  • Roulston T, Cane JH, Buchmann SL (2000) What governs protein content of pollen: pollinator preferences, pollen-pistil interactions, or phylogeny? Ecol Monogr 70:617–643

    Google Scholar 

  • Ruttner F, Hesse B (1981) Rassenspezifische Unterschiede in Ovarienentwicklung und Eiablage von weisellosen Arbeiterinnen der Honigbiene Apis mellifera L. Apidologie 12:159–183

    Article  Google Scholar 

  • Rutz W, Lüscher M (1974) The occurrence of vitellogenin in workers and queens of Apis mellifera and its transmission to the queen. J Insect Physiol 20:897–909

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Simon U, Moritz RFA, Crewe RM (2005) Reproductive dominance among honeybee workers in experimental groups of Apis mellifera capensis. Apidologie 36:413–419

    Article  Google Scholar 

  • Sakagami SF (1953) Untersuchungen über die Arbeitsteilung in einem Zwergvolk der Honigbiene. Beiträge zur Biologie des Bienenvolkes. Jap J Zool 11:117–185

    Google Scholar 

  • Sakagami SF (1958) The false queen: fourth adjustive response in dequeened honeybee colonies. Behaviour 13:280–296

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Stanley RG, Linskens HF (1974) Pollen: biology, biochemistry, management. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Velthuis HHW (1970) Ovarian development in Apis mellifera worker bees. Entomol Exp Appl 13:377–394

    Article  Google Scholar 

  • Velthuis HHW, Ruttner F, Crewe RM (1990) Differentiation in reproductive physiology and behaviour during the development of laying worker honeybees. In: Engels W (eds) Social Insects. Springer, Berlin Heidelberg New York, pp 231–243

    Google Scholar 

  • Visscher PK, Dukas R (1995) Honey bees recognise development of nestmates’ ovaries. Anim Behav 49:542–544

    Article  Google Scholar 

  • Vollbehr J (1975) Zur Orientierung junger Honigbienen bei ihrem 1. Orientierungsflug. Zool Jb Physiol 79:33–69

    Google Scholar 

  • Wheeler DE (1996) The role of nourishment in oogenesis. Ann Rev Entomol 41:403–431

    Article  Google Scholar 

  • Wilson EO (1971) The insect societies. Harvard University Press, Cambridge

    Google Scholar 

  • Wossler TC (2002) Pheromone mimicry by Apis mellifera capensis social parasites leads to reproductive anarchy in host Apis mellifera scutellata colonies. Apidologie 33:139–163

    Article  CAS  Google Scholar 

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Acknowledgments

Appreciation is addressed to Jürgen Liebig for support in the beginning of this study and to Thomas Mürrle for his technical assistance. We thank two anonymous referees for their constructive comments. Financial support was granted by a DAAD fellowship (MS), an Emmy Noether fellowship of the DFG (PN), the Volkswagen Foundation, the National Research Foundation of South Africa and the University of Pretoria (CP, VD and RC). The experiments comply with the “Principles of animal care”, publication No. 86–23, revised 1985 of the National Institute of Health, and with the current laws of South Africa where the experiments were performed.

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Authors and Affiliations

  1. Chemisches und Veterinäruntersuchungsamt Freiburg, Am Moosweiher 2, 79108, Freiburg, Germany

    M. O. Schäfer

  2. Department of Zoology and Entomology, University of Pretoria, 0002, Pretoria, South Africa

    V. Dietemann, C. W. W. Pirk & R. M. Crewe

  3. Institut für Zoologie, Martin-Luther-Universität Halle-Wittenberg, Hoher Weg 4, 06099, Halle (Saale), Germany

    P. Neumann

  4. Department of Zoology and Entomology, Rhodes University, 6140, Grahamstown, South Africa

    P. Neumann & H. R. Hepburn

  5. Bee-group, Biozentrum der Universität Würzburg, Am Hubland, 97074, Würzburg, Germany

    J. Tautz

  6. Institut für Zoologie, Universität Graz, Universitätsplatz 2, 8010, Graz, Austria

    K. Crailsheim

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  1. M. O. Schäfer
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  2. V. Dietemann
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  3. C. W. W. Pirk
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  4. P. Neumann
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  8. K. Crailsheim
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Correspondence to M. O. Schäfer.

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Schäfer, M.O., Dietemann, V., Pirk, C.W.W. et al. Individual versus social pathway to honeybee worker reproduction (Apis mellifera): pollen or jelly as protein source for oogenesis?. J Comp Physiol A 192, 761–768 (2006). https://doi.org/10.1007/s00359-006-0112-y

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  • DOI: https://doi.org/10.1007/s00359-006-0112-y

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