Temporal Memory in Foraging of the Stingless Bee Melipona subnitida (Hymenoptera: Apidae: Meliponini)


  • Albeane Guimarães Silva Programa de Pós-Graduação Biodiversidade e Biotecnologia da Rede Bionorte, São Luís, MA, Brasil; Programa de Pós Graduação de Biodiversidade e Conservação - Universidade Federal do Maranhão; Laboratório de Estudos sobre Abelhas, Universidade Federal do Maranhão, São Luís - MA, Brasil
  • Gracy Chrisley Alencar Carvalho Programa de Pós Graduação de Biodiversidade e Conservação - Universidade Federal do Maranhão; Laboratório de Estudos sobre Abelhas, Universidade Federal do Maranhão, São Luís - MA, Brasil
  • Ana Catarina de Miranda Programa de Pós-Graduação em Biodiversidade e Conservação, Universidade Federal do Maranhão, São Luís - MA, Brasil; Programa de Pós-Graduação em Neurociências e Comportamento, Universidade Federal do Pará, Belém - PA, Brasil
  • Felipe Andrés León Contrera Laboratório de Biologia e Ecologia de Abelhas, Instituto de Ciências Biológicas, Universidade Federal do Pará, Belém - PA, Brasil
  • Márcia Maria Corrêa Rêgo Programa de Pós-Graduação Biodiversidade e Biotecnologia da Rede Bionorte, São Luís, MA, Brasil; Programa de Pós Graduação de Biodiversidade e Conservação - Universidade Federal do Maranhão; Laboratório de Estudos sobre Abelhas, Universidade Federal do Maranhão, São Luís - MA, Brasil




Food-anticipatory activity, food resource, inspectors, reactivated, individual consistency, foragers


Bees feed on nectar and pollen, however these resources are often available to floral visitors during restricted temporal windows. The presence of temporal memory is an advantage, as foragers can save energy by scheduling their flight activity to coincide with peaks of nectar secretion in the flowers or at times of higher sugar concentration in the nectar. Thus, the objectives of this study were (i) to investigate whether Melipona subnitida has temporal memory, and evaluate whether it becomes more accurate over the days, and (ii) to determine whether the behavior of anticipating the offered resource presents intra-individual consistency in the behavior of foragers. The visitation of the bees was high before and during the opening interval of the food resource, but rare after the closing, suggesting that M. subnitida has the ability to memorize the time of availability of the resource, increasing the accuracy over the days, with bees anticipating their visits in relation to the time they discovered the resource, and the opening time of the resource. There was individual consistency in the behavior of food-anticipatory activity, with the presence of bees that consistently anticipated in relation to the opening time of the resource (inspectors) and bees that consistently did not anticipate (reactivated forager) . By anticipating the search for a resource, foragers allow the group to exploit it effectively, as they exploit it in the first hours of its opening, and foragers that never anticipate avoid unnecessary risks of predation and energy expenditure.


Aschoff, J. (1986). Anticipation of a daily meal: a process of ‘learning’ due to entrainment. Monitore Zoologico Italiano-Italian Journal of Zoology, 20: 195-219.

Barbosa, M.M., Bonatti, V., Teixeira, J.S.G., Rêgo, M.M.C. & Francoy, T.M. (2019). Genetic Characterization of Melipona subnitida Stingless Bee in Brazilian Northeast. Sociobiology, 66: 597-601. doi: 10.13102/sociobiology.v66i4.3408

Biesmeijer, J.C., van Nieuwstadt, M.G.L., Lukács, S. & Sommeijer, M.J. (1998). The role of internal and external information in foraging decisions of Melipona workers (Hymenoptera: Meliponinae). Behavioral Ecology and Sociobiology, 42: 107-116. doi: 10.1007/s002650050418

Biesmeijer, J.C. & Slaa, E.J. (2004). Information flow and organization of stingless bee foraging. Apidologie, 35: 143-157. doi: 10.1051/apido:2004003

Biesmeijer, J.C. & van Vries, H. (2001). Exploration and exploitation of food sources by social insect colonies: a revision of the scout-recruit concept. Behavioral Ecology and Sociobiology, 49: 89-99. doi: 0.1007/s002650000289

Breed, M.D., Stocker, E.M., Baumgartner, L.K. & Vargas, S.A. (2002). Time-place learning and the ecology of recruitment in a stingless bee, Trigona amalthea (Hymenoptera, Apidae). Apidologie, 33: 251-258. doi: 10.1051/apido:2002018

Bruijn, L.L.M. & Sommejer, M.J. (1997) Colony foraging in different species of stingless bees (Apidae, Meliponini) and the regulation of individual nectar foraging. Insectes Sociaux, 44: 35-47.

Corbet, S.A. & Delfosse, E.S. (1984). Honeybees and the nectar of Echium plantagineum L. in southeastern Australia. Australian Journal of Ecology, 9: 125-139. doi: 10.1111/j.1442-9993. 1984.tb01351.x

Correia, F.C.S, Peruquetti, R.C., da Silva, A.R. & Gomes, F.A. (2017). Influência da temperatura e umidade nas atividades de vôo de operárias de Melipona eburnea (Apidae, Meliponina). Arquivos de Ciências Veterinárias e Zoologia da UNIPAR, 20: 65-70.

Diniz, M.R., Silva, A.G., Carreira, L.M.M., Almeida Jr, E.B.D. & Rêgo, M.M.C. (2021). Pollen Spectrum of Honey from the Bee Melipona subnitida Ducke (1910) in Restinga in Maranhão State. Floresta e Ambiente, 28: e20200068 doi: 10.1590/ 2179-8087-FLORAM-2020-0068

Dornhaus, A. & Chittka, L. (2004). Information flow and regulation of foraging activity in bumble bees (Bombus spp.). Apidologie, 35: 183-192. doi:10.1051/apido:2004002

Edge, A.A., Van Nest, B.N., Johnson, J.N., Miller, S.N., Naeger, N.L., Boyd, S.D. & Moore, D. (2012) Diel nectar secretion rhythm in squash (Cucurbita pepo) and its relation with pollinator activity. Apidologie, 43: 1-16. doi: 10.1007/s13592-011-0087-8

Granovskiy, B., Latty, T., Duncan, M., Sumpter, D.J.T., & Beekman, M. (2012). How dancing honey bees keep track of changes: the role of inspector bees. Behavioral Ecology, 23: 588-596. doi: 10.1093/beheco/ars002

Gould, J.L. (1987). Honey bees store learned flower landing behaviour according to time of day. Animal Behaviour, 35: 1579-1581. doi: 10.1016/S0003-3472(87)80038-6

Hubbell, S.P. & Johnson, L.K. (1978). Comparative foraging behavior of six stingless bee species exploiting a standardized resource. Ecology, 59: 1123-1136

Hrncir, M., Jarau, S., Zucchi, R. & Barth, F.G. (2000). Recruitment behavior in stingless bees, Melipona scutellaris and M. quadrifasciata. II. Possible mechanisms of communication. Apidologie, 31: 93-113. doi: 10.1051/apido:2000109

Jammalamadaka, S.R. & SenGupta, A. (2001). Topics in circular statistics. World Scientific Publication, NJ

Jarau, S., Hrncir, M., Schmidt, V. M., Zucchi, R. & Barth, F.G. (2003). Effectiveness of recruitment behavior in stingless bees (Apidae, Meliponini). Insectes Sociaux, 50: 365-374. doi: 10.1007/s00040-003-0684-2

Jarau, S. (2009). Chemical communication during food exploitation in stingless bees. In: Jarau S, Hrncir M (eds) Food exploitation by social insects. Ecological, behavioral, and theoretical approaches.CRC, Boca Raton, pp 223-249

Jesus, T.N.C.S., Venturieri, G.C. & Contrera, F.A.L. (2014). Time-place learning in the bee Melipona fasciculata (Apidae, Meliponini). Apidologie, 45: 257-265. doi: 10.1007/s13592-013-0245-2

Maia-Silva, C., Hrncir, M., Silva, C.I. & Imperatriz-Fonseca, V.L. (2015). Survival strategies of stingless bees (Melipona subnitida) in an unpredictable environment, the Brazilian tropical dry Forest. Apidologie, 46: 631-643. doi: 10.1007/s13592-015-0354-1

Matile, P. (2006). Circadian rhythmicity of nectar secretion in Hoya carnosa. Botanica Helvetica, 116: 1-7. doi: 10.1007/s00035-006-0740-4

Michener, C.D. (2007). The bees of the Word. 2 ed. The Johns Hopkins University Press, Baltimore

Moore, D. & Doherty, P. (2009). Acquisition of a time-memory in forager honey bees. Journal of Comparative Physiology, 195: 741-751. doi: 10.1007/s00359-009-0450-7

Moore, D. & Rankin, M.A. (1983). Diurnal changes in the accuracy of the honeybee foraging rhythm. The Biological Bulletin, 164: 471-482.

Moore, D., Rankin, M.A. (1985). Circadian locomotor rhythms in individual honeybees. Physiological Entomology, 10: 91-197.

Moore, D., Van Nest, B.N. & Seier, E. (2011). Diminishing returns: the influence of experience and environment on time-memory extinction in honey bee foragers. Journal of Comparative Physiology A, 197: 641-651. doi: 10.1007/s00359-011-0624-y

Murphy, C.M. & Breed, M.D. (2008). Time-place learning in a neotropical stingless bee, Trigona fulviventris Guérin (Hymenoptera: Apidae). Journal of the Kansas Entomological Society, 81: 73-76. doi: 10.2317/JKES-704.23.1

Nakagawa, S. & Schielzeth, H. (2010). Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biological Reviews, 85: 935-956. doi: 10.1111/j.1469-185X. 2010.00141.x

Nieh, J.C. (2004). Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie, 35: 159-182. doi: 10.1051/apido:2004007

Nieh, J.C., Barreto, L.S., Contrera, F.A. & Imperatriz-Fonseca, V.L. (2004). Olfactory eavesdropping by a competitively foraging stingless bee, Trigona spinipes. Proceedings of the Royal Society of London. Series B: Biological Sciences, 271: 1633-1640. doi: 10.1098/rspb.2004.2717

Pierrot, L.M. & Schlindwein, C. (2003). Variation in daily flight activity and foraging patterns in colonies of uruçu Melipona scutellaris Latreille (Apidae, Meliponini). Revista Brasileira de Zoologia, 20: 565-571.

Pinter-Wollman, N. (2012). Personality in social insects: How does worker personality determine colony personality? Current Zoology, 58: 579-587. doi: 10.1093/czoolo/58.4.580

Pinto, R.S., Albuquerque, P.M.C., Rêgo, M.M.C. (2014). Pollen analysis of food pots stored by Melipona subnitida Ducke (Hymenoptera: Apidae) in a restinga area. Sociobiology, 61: 461-469. doi: 10.13102/sociobiology.v61i4.461-469

Pinto, R.S., Rêgo, M.M.C. & Albuquerque, P.M.C. (2020). Honey pollen spectra of two species of stingless bee (Apidae: Meliponini) in Lençóis Maranhenses National Park, Brazil. Grana, 1-14. doi: 10.1080/00173134.2020.1821088

Poctor, M., Yeu, P., Lack, A. (1996). The natural of history of pollination. Harper Collins, London.

R Development Core Team (2020). R: A Language and Environment for Statistical Computing. Brazil, R foundation for statisticalcomputing, Rio de Janeiro.

Rios, L. (2001). Estudos de Geografia do Maranhão.Graphis editora, São Luís.

Roubik, D.W. (1989). Ecology and natural history of tropical bees. Cambridge University Press, New York.

Seeley, T.D., Camazine, S. & Sneyd, J. (1991). Collective decision-making in honey bees: how colonies choose among nectar sources. Behavioral Ecology and Sociobiology, 28: 277-290. doi: 10.1007/BF00175101

Silva, A.G., Pinto, R.S., Contrera, F.A.L., Albuquerque, P.M.C. & Rêgo, M.M.C. (2014). Foraging distance of Melipona subnitida Ducke (Hymenoptera: Apidae). Sociobiology, 61: 494-501.

Statsoft Inc. (2004). Statistica (data analysis software system), version 7.

van Doorn, W.G. & van Meeteren, U. (2003). Flower opening and closure: a review. Journal of Experimental Botany, 54: 1801-1812. doi: 10.1093/jxb/erg213

van Nest, B.N. & Moore, D. (2012). Energetically optimal foraging strategy is emergent property of time-keeping behavior in honey bees. Behavioral Ecology, 23: 649-658. doi: 10.1093/beheco/ars010

Venturieri, G.C. (2008). Caixa para a criação de Uruçu Amarela Melipona flavolineata Friese, 1900. Comunicado Técnico Embrapa Amazônia Oriental, 212: 1-8.

von Frisch, K. (1967). The dance language and orientation of bees. Harvard University Press, Cambridge.

von Frisch, B. & Aschoff, J. (1987). Circadian rhythms in honeybees: entrainment by feeding cycles. Physiological Entomology, 12: 41-49. doi: 10.1111/j.1365-3032.1987.tb00722.x

Wagner, A.E., Van Nest, B.N., Hobbs, C.N. & Moore, D. (2013). Persistence, reticence and the management of multiple time memories by forager honey bees. Journal of Experimental Biology, 216: 1131-1141. doi: 10.1242/jeb.064881

Willmer, P.G. & Corbet, S.A. (1981). Temporal and microclimatic partitioning of the floral resources of Justicia aurea amongst a concourse of pollen vectors and nectar robbers. Oecologia, 51: 67-78.

Zanella, F.C.V. (2000). The bees of the Caatinga (Hymenoptera, Apoidea, Apiformes): A species list and comparative notes regarding their distribution. Apidologie, 31: 579-592. doi: 10.1051/apido:2000148

Zar, J.H. (1999). Biostatistical analysis. Prentice Hall, New Jersey.




How to Cite

Guimarães Silva, A., Carvalho, G. C. A., de Miranda, A. C., Contrera, F. A. L., & Rêgo, M. M. C. (2021). Temporal Memory in Foraging of the Stingless Bee Melipona subnitida (Hymenoptera: Apidae: Meliponini). Sociobiology, 68(2), e5863. https://doi.org/10.13102/sociobiology.v68i2.5863



Research Article - Bees

Most read articles by the same author(s)