Insectes Sociaux

, Volume 65, Issue 3, pp 465–471 | Cite as

Cooperation and antagonism over time: a conflict faced by males of Tetragonisca angustula in nests

  • C. F. dos SantosEmail author
Research Article


Before leaving to look for mates, the male stingless bees seem to face a dilemma to obtain food (energy) while avoiding aggression from the workers in their natal nests. It has been theorised that if these males waste time managing both situations inside the nests, it could reduce their chances of inseminating virgin queens outside nests. Here, I study Tetragonisca angustula (Hymenoptera: Apidae: Meliponini) males as a model of stingless bees to analyse whether the number of positive and negative interactions (cooperation = trophallaxis; antagonism = bites, respectively) with their worker nestmates are affected by the number of males inside nests or then by the time spent by them there. Next, I evaluate the binomial probability of these males leaving their natal nests as a function of trophallaxis and bites received of the workers. Finally, I assess which of the males’ body parts are commonly bitten by workers. The results demonstrate that males join with other males every day in hot places inside the nests to dehydrate nectar. Paradoxically, both trophallaxis and bites (these are often on legs) received from workers rise significantly throughout the time spent in the nests. Then, the probability of males leaving their natal nests rises 85% for every day spent inside the colonies. These data reinforce the suggestion of a dilemma faced by T. angustula males with relation to when to leave, i.e. how long to spend obtaining energy (and safety) within the nests while enduring aggression from workers, before permanently abandoning their natal nests to look for mates.


Aggression Interaction behaviour Social insects Tropical bees Trophallaxis 



The author is grateful to Kedar Devkota for critical reading and suggestions to the manuscript. The author would also like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES/PROEX; CAPES/PNPD) for financial support.

Supplementary material

40_2018_633_MOESM1_ESM.pdf (666 kb)
Supplementary material 1 (PDF 665 KB)


  1. Alcock J, Barrows EM, Gordh G et al (1978) The ecology and evolution of male reproductive behaviour in the bees and wasps. Zool J Linn Soc 64:295–326CrossRefGoogle Scholar
  2. Ayasse M, Paxton RJ, Tengö J (2001) Mating behavior and chemical communication in the order Hymenoptera. Annu Rev Entomol 46:31–78CrossRefPubMedGoogle Scholar
  3. Bates D, Maechler M, Bolker B, Walker S (2015) lme4: Linear mixed-effects models using Eigen and S4Google Scholar
  4. Beani L, Dessì-Fulgheri F, Cappa F, Toth A (2014) The trap of sex in social insects: from the female to the male perspective. Neurosci Biobehav Rev 46:519–533. CrossRefPubMedGoogle Scholar
  5. Bego LR, Grosso AF, Zucchi R, Sakagami SF (1999) Oviposition behavior of the stingless bees XXIV. Ethological relationships of Tetragonisca angustula angustula to other Meliponinae taxa (Apidae: Meliponinae). Entomol Sci 2:473–482Google Scholar
  6. Bertsch A (1984) Foraging in male bumblebees (Bombus lucorum L.): maximizing energy or minimizing water load? Oecologia 62:325–336. CrossRefPubMedGoogle Scholar
  7. Camargo CA (1972) Mating of the social bee Melipona quadrifasciata under controlled conditions (Hymenoptera, Apidae). J Kansas Entomol Soc 45:520–523Google Scholar
  8. Carvalho GA, Kerr WE, Nascimento VA (1995) Sex determination in bees. XXXIII. Decrease of xo hetero-alleles in a finite population of Melipona scutellaris (Apidae, Meliponinae). Braz J Genet 18Google Scholar
  9. Cortopassi-Laurino M (2007) Drone congregations in Meliponini: what do they tell us? Biosci J 23:153–160Google Scholar
  10. Cortopassi-Laurino M (1979) Observações sobre atividades de machos de Plebeia droryana Friese (Apidae, Meliponinae). Rev Bras Entomol 23:177–191Google Scholar
  11. Costa JT, Fitzgerald TD (2005) Social terminology revisited: Where are we ten years later? Ann Zool Fennici 42:559–564Google Scholar
  12. Craig R (1982) Evolution of male workers in the Hymenoptera. J Theor Biol 94:95–105CrossRefGoogle Scholar
  13. Darvill B, Lye GC, Goulson D (2007) Aggregations of male Bombus muscorum (Hymenoptera: Apidae) at mature nests. Incestuous brothers or amorous suitors? Apidologie 38:518–524. CrossRefGoogle Scholar
  14. dos Santos CF, Ferreira-Caliman MJ, Nascimento FS (2015) An alien in the group: eusocial male bees sharing nonspecific reproductive aggregations. J Insect Sci 15:157–163. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Foster RL (1992) Nestmate recognition as an inbreeding avoidance mechanism in bumble bees (Hymenoptera: Apidae). J Kansas Entomol Soc 65:238–243Google Scholar
  16. Francini IB, Nunes-Silva CG, Carvalho-Zilse GA (2012) Diploid male production of two amazonian Melipona bees (Hymenoptera: Apidae). Psyche (Stuttg) 1–7.
  17. Goins A, Schneider SS (2013) Drone “quality” and caste interactions in the honey bee, Apis mellifera L. Insectes Soc 60:453–461. CrossRefGoogle Scholar
  18. Grosso AF, Bego LR (2000) The production of males in queenright colonies of Tetragonisca angustula angustula (Hymenoptera, Meliponinae). Sociobiology 35:475–485Google Scholar
  19. Hervé M (2015) RVAideMemoire: Diverse basic statistical and graphical functionsGoogle Scholar
  20. Imperatriz-Fonseca VL (1973) Miscellaneous observations on the behaviour of Schwarziana quadripunctata (Hymenoptera, Apidae, Meliponinae). Bol Zool e Biol Mar 30:633–640CrossRefGoogle Scholar
  21. Imperatriz-Fonseca VL (1977) Studies on Paratrigona subnuda (Moure) (Hymenoptera, Apidae, Meliponinae) – II. Behaviour of the virgin Queen. Bol Zool da Univ São Paulo 2:169–182Google Scholar
  22. Kerr WE (1990) Why are workers in social Hymenoptera not males. Brazilian J Genet 13:133–136Google Scholar
  23. Kerr WE, Zucchi R, Nakadaira JT, Butolo JE (1962) Reproduction in the social bees (Hymenoptera: Apidae). J N Y Entomol Soc 70:265–276Google Scholar
  24. Koedam D, Velthausz PH, VanderKrift T et al (Apidae (1996) Morphology of reproductive and trophic eggs and their controlled release by workers in Trigona (Tetragonisca) angustula Illiger. Meliponinae). Physiol Entomol 21:289–296. CrossRefGoogle Scholar
  25. Koeniger N, Koeniger G, Gries M, Tingek S (2005) Drone competition at drone congregation areas in four Apis species. Apidologie 36:211–221. CrossRefGoogle Scholar
  26. Michener CD (1969) Comparative social behavior of bees. Annu Rev Entomol 14:299–342CrossRefGoogle Scholar
  27. Nunes TM, Oldroyd BP, Elias LG et al (2017) Evolution of queen cuticular hydrocarbons and worker reproduction in stingless bees. Nat Evol Ecol 1:1–3. CrossRefGoogle Scholar
  28. Paxton RJ (2005) Male mating behaviour and mating systems of bees: an overview. Apidologie 36:145–156. CrossRefGoogle Scholar
  29. R Core Team (2016) R: A language and environment for statistical computing. The R Foundation for Statistical Computing, ViennaGoogle Scholar
  30. Roig-Alsina A, Michener CD (1993) Studies of the phylogeny and classification of long-tongued bees (Hymenoptera: Apoidea). Univ kansas Sci Bull 55:123–173CrossRefGoogle Scholar
  31. Roubik DW (1990) Mate location and mate competition in males of stingless bees (Hymenoptera: Apidae: Meliponinae). Entomol Gen 15:115–120CrossRefGoogle Scholar
  32. Sakagami SF (1982) Stingless bees. In: Hermann HR (ed) Social Insects. New Yourk Academic Press, New York, pp 361–423CrossRefGoogle Scholar
  33. Sakagami SF, Laroca S (1963) Additional observations on the habits of the cleptobiotic stingless bees, the Genus Lestrimelitta Friese (Hymenoptera, Apoidea). J Fac Sci Hokkaido Univ Ser VI Zool 15:319–339Google Scholar
  34. Santos CF, Menezes C, Vollet-Neto A, Imperatriz-Fonseca VL (2014) Congregation sites and sleeping roost of male stingless bees (Hymenoptera: Apidae: Meliponini). Sociobiology 61:115–118. CrossRefGoogle Scholar
  35. Schwarz HF (1948) Stingless bees (Meliponidae) of the Western Hemisphere: Lestrimelitta and the following subgenera of Trigona: Trigona, Paratrigona, Schwarziana, Parapartamona, Cephalotrigona, Oxytrigona, Scaura, and Mourella. Bull Am Museum Nat Hist 90:1–546Google Scholar
  36. Sommeijer MJ, Bruijn LLM, Meeuwsen FJAJ. (2003) Reproductive behaviour of stingless bees: solitary gynes of Melipona favosa (Hymenoptera: Apidae, Meliponini) can penetrate existing nests. Entomol Ber 63:31–35Google Scholar
  37. Starr CK (1985) What if workers in social Hymenoptera were males? J Theor Biol 117:11–18CrossRefGoogle Scholar
  38. Stout TL, Slone JD, Schneider SS (2011) Age and behavior of honey bee workers, Apis mellifera, that interact with drones. Ethology 117:459–468. CrossRefGoogle Scholar
  39. van Veen JW, Sommeijer MJ, Meeuwsen F (1997) Behaviour of drones in Melipona (Apidae, Meliponinae). Insectes Soc 44:435–447. CrossRefGoogle Scholar
  40. Wilson EO (1971) The insect societies. Harvard University Press, CambridgeGoogle Scholar
  41. Wilson EO, Holldobler B (2005) Eusociality: origin and consequences. Proc Natl Acad Sci U S A 102:13367–13371CrossRefPubMedPubMedCentralGoogle Scholar
  42. Wittmann D, Scholz E (1989) Nectar dehydration by male carpenter bees as preparation for mating flights. Behav Ecol Sociobiol 25:387–391CrossRefGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2018

Authors and Affiliations

  1. 1.Department of Ecology, Biosciences InstituteUniversity of São Paulo, USPSão PauloBrazil
  2. 2.Department of Biodiversity and Ecology, School of Biological SciencesPontifical Catholic University of Rio Grande do Sul, PUCRSPorto AlegreBrazil

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