Diapause in Stingless Bees (Hymenoptera: Apidae)


  • Charles Fernando dos Santos Pontifícia Universidade Católica do Rio Grande do Sul
  • Patrícia Nunes-Silva Pontifícia Universidade Católica do Rio Grande do Sul
  • Rosana Halinski Pontifícia Universidade Católica do Rio Grande do Sul
  • Betina Blochtein Pontifícia Universidade Católica do Rio Grande do Sul




Plebeia, provisioning and oviposition process, reproductive diapause, temperature, photoperiodism


Extreme environmental conditions may negatively affect development animals which present behavior strategies in order survivor them. Insects present a wide range of adaptive behaviors that have allowed them to successfully respond to adverse climatic conditions by temporarily interrupting some of their activities or development. One of these behaviors is diapause. It is a gradual and progressive interruption in development or ontogeny of any organism in some phase of their lifecycle in order to survivor unfavorable environmental conditions that occur cyclically. The objective of this review is to give an overview of the current knowledge about diapause in stingless bees and future perspectives of study. It focuses on Plebeia Schwarz species because this behavior has been observed mainly in these bees. In this group of bees there is a stop in the provisioning and oviposition process in autumn/winter, called reproductive diapause. Besides the stop in brood rearing, other behaviors, as for example foraging, are modified. The mechanisms that induce the reproductive diapause are still unclear, but the evidence points out to the temperature and photoperiodism as the main drivers of this behavior.


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Author Biographies

Charles Fernando dos Santos, Pontifícia Universidade Católica do Rio Grande do Sul

Departamento de Biodiversidade e Ecologia, Faculdade de Biociências

Patrícia Nunes-Silva, Pontifícia Universidade Católica do Rio Grande do Sul

Departamento de Biodiversidade e Ecologia, Faculdade de Biociências

Rosana Halinski, Pontifícia Universidade Católica do Rio Grande do Sul

Departamento de Biodiversidade e Ecologia, Faculdade de Biociências

Betina Blochtein, Pontifícia Universidade Católica do Rio Grande do Sul

Departamento de Biodiversidade e Ecologia, Faculdade de Biociências


Adedokun, T. A., & Denlinger, D. L. (1985). Metabolic reserves associated with pupal diapause in the

flesh fly, Sarcophaga crassipalpis. Journal of Insect Physiology, 31: 229–233.

Alves, D. A., Imperatriz-Fonseca, V. L., & Santos-Filho, P. S. (2009). Production of workers, queens and

males in Plebeia remota colonies (Hymenoptera, Apidae, Meliponini), a stingless bee with reproductive

diapause. Genetics and Molecular Research, 8: 672–683.

Beekman, M., van Stratum, P., & Lingeman, R. (1998). Diapause survival and post-diapause performance

in bumblebee queens (Bombus terrestris). Entomologia Experimentalis et Applicata, 89: 207–214.

Bloch, G., Herzog, E. D., Levine, J. D., & Schwartz, W. J. (2013). Socially synchronized circadian

oscillators. Proceedings of the Royal Society B: Biological Sciences, 280: 20130035. doi:


Blochtein, B., Witter, S., & Imperatriz–Fonseca, V. L. (2008). Adaptações das abelhas sem ferrão ao

clima temperado do sul do Brasil. In D. de Jong, T. M. Francoy, & W. C. Santana (Eds.), Anais do VIII

Encontro sobre Abelhas (pp. 121–130). Ribeirão Preto: FUNPEC.

Borges, F. V. B., & Blochtein, B. (2006). Variação sazonal das condições internas de colônias de

Melipona marginata obscurior Moure, no Rio Grande do Sul, Brasil. Revista Brasileira de Zoologia,

: 711–715.

Bosch, J., Sgolastra, F., & Kemp, W. P. (2010). Timing of eclosion affects diapause development, fat

body consumption and longevity in Osmia lignaria, a univoltine, adult-wintering solitary bee. Journal of

Insect Physiology, 56: 1949–1957. doi:10.1016/j.jinsphys.2010.08.017.

Camargo, J. M. F., & Pedro, S. R. M. (1992). Systematics, phylogeny and biogeography of the

Meliponinae (Hymenoptera, Apidae). Apidologie, 23: 509–522.

Camargo, J. M. F., & Pedro, S. R. M. (2013). Meliponini Lepeletier, 1836. In J. S. Moure, D. Urban, & G.

A. R. Melo (Eds.), Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region - online version.

http://www.moure.cria.org.br/catalogue. (accessed date: 15 september, 2014)

Chen, C., Xia, Q.-W., Fu, S., Wu, X.-F., & Xue, F.-S. (2014). Effect of photoperiod and temperature on

the intensity of pupal diapause in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). Bulletin of Entomological Research, 104: 12–18. doi:10.1017/S0007485313000266.

Denlinger, D. L. (1986). Dormancy in tropical insects. Annual Review of Entomology, 31: 239–264.


Denlinger, D. L. (2002). Regulation of diapause. Annual Review of Entomology, 47: 93–122.


Derr, J. A. (1980). Coevolution of the life history of a tropical seed-feeding insect and its food plants.

Ecology, 61: 881–892. doi:10.2307/1936758.

Drumond, P. M., Bego, L. R., & Zucchi, R. (1997). Oviposition behavior of the stingless bees XIX.

Plebeia (Plebeia) poecilochroa with highly integrated oviposition process and small colony size

(Hymenoptera, Apidae, Meliponinae). Japanese Journal of Entomolgy, 65: 7–22.

Drumond, P. M., Zucchi, R., Mateus, S., & Bego, L. R. (1996). Oviposition behavior of the stingless bees

XVII. Plebeia (Plebeia) droryana and a ethological comparison with other Meliponinae taxa

(Hymenoptera, Apidae). Japanese Journal of Entomolgy, 64: 385–400.

Drumond, P. M., Zucchi, R., & Oldroyd, B. P. (2000). Description of the cell provisioning and oviposition

process of seven species of Plebeia Schwarz (Apidae, Meliponini), with notes on their phylogeny and

taxonomy. Insectes Sociaux, 47: 99–112. doi:10.1007/PL00001703.

Drumond, P. M., Zucchi, R., Yamase, S., & Sakagami, S. F. (1996). Oviposition behavior of the stingless

bees XVIII. Plebeia (Plebeia) emerina and P. (P.) remota with a preliminary ethological comparison of

some Plebeia taxa (Apidae, Meliponinae). The Bulletin of the Faculty of Education, 45: 31–55.

Drumond, P. M., Zucchi, R., Yamase, S., & Sakagami, S. F. (1998). Oviposition behavior of the stingless

bees XX. Plebeia (Plebeia) julianii with forms very small brood batches (Hymenoptera, Apidae,

meliponinae). Entomological Science, 1: 195–205.

Fliszkiewicz, M., Giejdasz, K., Wasielewski, O., & Krishnan, N. (2012). Influence of winter temperature

and simulated climate change on body mass and fat body depletion during diapause in adults of the

solitary bee, Osmia rufa (Hymenoptera: Hymenoptera). Environmental Entomology, 41: 1621–1630.


Freitas, B. M., Imperatriz-Fonseca, V. L., Medina, L. M., Kleinert, A. M. P., Galetto, L., Nates-Parra, G.,

& Quezada-Euán, J. J. G. (2009). Diversity, threats and conservation of native bees in the Neotropics.

Apidologie, 40: 332–346. doi:10.1051/apido/2009012

Gallai, N., Salles, J.-M., Settele, J., & Vaissière, B. E. (2009). Economic valuation of the vulnerability of

world agriculture confronted with pollinator decline. Ecological Economics, 68: 810–821.


Giannini, T. C., Acosta, A. L., Garófalo, C. A., Saraiva, A. M., Alves-dos-Santos, I., & Imperatriz

Fonseca, V. L. (2012). Pollination services at risk: Bee habitats will decrease owing to climate change in

Brazil. Ecological Modelling, 244: 127–131. doi:10.1016/j.ecolmodel.2012.06.035.

Goulson, D. (2010). Bumblebees: behaviour, ecology, and conservation. (second., p. 317). New York:

Oxford University Press.

Greenfield, M. D., & Pener, M. P. (1992). Alternative schedules of male reproductive diapause in the

grasshopper Anacridium aegyptium (L.): effects of the corpora allata on sexual behavior (Orthoptera:

Acrididae). Journal of Insect Behavior, 5: 245–261.

Herman, W. S. (1981). Studies on the adult reproductive diapause of the monarch butterfly, Danaus

perxippus. Biological Bulletin, 160: 89–106.

Hsiao, C., & Hsiao, T. H. (1969). Insect hormones: their effects on diapause and development of

Hymenoptera. Life Sciences, 8: 767–774.

Imperatriz-Fonseca, V. L., & Oliveira, M. A. C. (1976). Observations on a queenless colony of Plebeia

saiqui (Friese) (Hymenoptera, Apidae, Meliponinae). Boletim de Zoologia Universidade de São Paulo, 1:


Instituto Nacional de Metereologia [INMET]. (2014).

http://www.inmet.gov.br/portal/index.php?r=home2/index (accessed date: 18 September, 2014)

Jones, J. C., & Oldroyd, B. P. (2006). Nest thermoregulation in social insects. Advances in Insect

Physiology, 33: 143–191. doi:10.1016/S0065-2806(06)33003-2

Juliani, L. A. (1967). Descrição do ninho e alguns dados biológicos sobre a abelha Plebeia julianii Moure,

(Hymenoptera, Apidae, Meliponinae). Revista Brasileira de Entomologia, 12: 31–58.

Kimura, M. T. (1988). Interspecific and geographic variation of diapause intensity and seasonal adaptation

in the Drosophila auraria species complex (Diptera: Drosophilidae). Functional Ecology, 2: 177–183.

Kipyatkov, V. E. (2001). A distantly perceived primer pheromone controls diapause termination in the ant

Myrmica rubra L. (Hymenoptera, Formicidae). Journal of Evolutionary Biochemistry and Physiology,

: 405–416. doi:10.1023/A:1012926929059.

Kipyatkov, V. E., Lopatina, E. B., & Pinegin, A. Y. (1997). Social regulation of development and

diapause in the ant Leptothorax acervorum (Hymenoptera, Formicidae). Entomological Review, 77:


Kleinert-Giovannini, A. (1982). The influence of climatic factors on flight activity of Plebeia emerina

Friese (Hymenoptera, Apidae, Meliponinae) in winter. Revista Brasileira de Entomologia, 26: 1–13.

Kleinert-Giovannini, A., & Imperatriz–Fonseca, V. L. (1986). Flight activity and climatic conditions and

responses to climatic conditions by two subspecies of Melipona marginata Lepeletier (Apidae,

Meliponinae). Journal of Apicultural Research, 25: 3–8.

Kort, C. A. D. (1990). Thirty-five years of diapause research with the Colorado potato beetle.

Entomologia Experimentalis et Applicata, 56: 1–13.

Koštál, V. (2006). Eco-physiological phases of insect diapause. Journal of Insect Physiology, 52: 113


Lefevere, K. S., Koopmanschap, A. B., & de Kort, C. A. D. (1989). Juvenile hormone metabolism during

and after diapause in the female Colorado potato beetle, Leptinotarsa decemlineata. Journal of Insect

Physiology, 35: 129–135.

Nogueira-Neto, P. (1997). Vida e criação de abelhas indígenas sem ferrão (p. 445). São Paulo/ Brasil:

Editora Nogueirapis.

Nunes-Silva, P., Hilário, S. D., Santos Filho, P. S., & Imperatriz-Fonseca, V. L. (2010). Foraging activity

in Plebeia remota, a stingless bees species, is influenced by the reproductive state of a colony. Psyche, (i):

–16. doi:10.1155/2010/241204

Ollerton, J., Winfree, R., & Tarrant, S. (2011). How many flowering plants are pollinated by animals?

Oikos, 120: 321–326. doi:10.1111/j.1600-0706.2010.18644.x.

Pick, R. A., & Blochtein, B. (2002). Atividades de coleta e origem floral do polen armazenado em

colonias de Plebeia saiqui (Holmberg) (Hymenoptera, Apidae, Meliponinae) no sul do Brasil. Revista

Brasileira de Zoologia, 19: 289–300.

Pick, R. A., & Blochtein, B. (2002). Atividades de vôo de Plebeia saiqui (Holmberg) (Hymenoptera,

Apidae, Meliponini) durante o período de postura da rainha e em diapausa. Revista Brasileira de Zoologia,

: 827–839.

Plowright, R. C., & Laverty, T. M. (1984). The ecology and sociobiology of bumble bees. Annual Review

of Entomology, 29: 175–199.

Ribeiro, M. F. (2002). Does the queen of Plebeia remota (Hymenoptera, Apidae, Meliponini) stimulate her

workers to start brood cell construction after winter? Insectes Sociaux, 49: 38–40. doi:10.1007/s00040


Ribeiro, M. F., Imperatriz-Fonseca, V. L., & Santos-Filho, P. (2003). A interrupção da construção de

células de cria e postura em Plebeia remota (Holmberg) (Hymenoptera, Apidae, Meliponini). In G. A. R.

Melo & I. Alves-dos-Santos (Eds.), Apoidea Neotropica: homenagem aos 90 anos de Jesus Santiago

Moure (pp. 177–188). Criciúma: Editora UNESC.

Sakagami, S. F. (1982). Stingless bees. In H. R. Hermann (Ed.), Social Insects (pp. 361–423). New York:

New Yourk Academic Press.

Saunders, D. S. (2012). Insect photoperiodism: seeing the light. Physiological Entomology, 37: 207


Saunders, D. S. (2014). Insect photoperiodism: effects of temperature on the induction of insect diapause

and diverse roles for the circadian system in the photoperiodic response. Entomological Science, 17:

–40. doi:10.1111/ens.12059

Seeley, T. D. (1985). Honeybee ecology: a study of adaptation in social life. Princeton University Press.

Silveira, F. A., Melo, G. A. R., & Almeida, E. A. B. (2002). Abelhas brasileiras: sistemática e

identificação (p. 253). Belo Horizonte: Fundação Araucária.

Sung, I.-H., Yamane, S., & Hozumi, S. (2008). Thermal characteristics of nests of the Taiwanese stingless

bee Trigona ventralis hoozana (Hymenoptera: Apidae). Zoological Studies, 47: 417–428.

Takagi, S., & Miyashita, T. (2008). Host plant quality influences diapause induction of Byasa alcinous

(Lepidoptera: Papilionidae). Annals of the Entomological Society of America, 101: 392–396.

Tatar, M., & Yin, C. M. (2001). Slow aging during insect reproductive diapause: why butterflies,

grasshoppers and flies are like worms. Experimental Gerontology, 36: 723–738.

Tauber, E., & Kyriacou, B. P. (2001). Insect photoperiodism and circadian clocks: models and

mechanisms. Journal of Biological Rhythms, 16: 381–390. doi:10.1177/074873001129002088.

Tauber, M. J., & Tauber, C. A. (1976). Insect seasonality: diapause maintenance, termination, and

postdiapause development. Annual Review of Entomology, 21: 81-107.


Terada, Y., Garófalo, C. A., & Sakagami, S. F. (1975). Age-survival curves for workers of two eusocial

bees (Apis mellifera and Plebeia droryana) in a subtropical climate, with notes on worker polyethism in P.

droryana. Journal of Apicultural Research, 14: 161–170.

Togashi, K. (2014). Effects of larval food shortage on diapause induction and adult traits in Taiwanese

Monochamus alternatus alternatus. Entomologia Experimentalis et Applicata, 151: 34–42.


Van Benthem, F. D. J., Imperatriz–Fonseca, V. L., & Velthuis, H. H. W. (1995). Biology of the stingless

bee Plebeia remota (Holmberg): observations and evolutionary implications. Insectes Sociaux, 87: 71–87.


Vaz Nunes, M., & Saunders, D. S. (1989). The effect of larval temperature and photoperiod on the

incidence of larval diapause in the blowfly, Calliphora vicina. Physiological Entomology, 14: 471–474.


Wasielewski, O., Wojciechowicz, T., Giejdasz, K., & Krishnan, N. (2013). Overwintering strategies in the

red mason solitary bee—physiological correlates of midgut metabolic activity and turnover of nutrient

reserves in females of Osmia bicornis. Apidologie, 44: 642–656. doi:10.1007/s13592-013-0213-x.

Witter, S., Blochtein, B., Andrade, F., Wolff, L. F., & Imperatriz–Fonseca, V. L. (2007). Meliponicultura no Rio Grande do Sul: contribuição sobre a biologia e conservação de Plebeia nigriceps (Friese 1901) (Apidae, Meliponini). Bioscience Journal, 23: 134–140.

Wittmann, D. (1989). Nest architecture, nest site preferences and distribution of Plebeia wittmanni (Moure

& Camargo, 1989) in Rio Grande do Sul, Brazil (Apidae: Meliponinae). Studies on Neotropical Fauna and

Environment, 24: 17–23.doi:10.1080/01650528909360771.

Zucchi, R. (1993). Ritualized dominance, evolution of queen-worker interactions and related aspects in

stingless bees (Hymenoptera: Apidae). In T. Inoue & S. Yamane (Eds.), Evolution of insect societies (pp.

–249). Tokyo: Hakuhinsha.




How to Cite

dos Santos, C. F., Nunes-Silva, P., Halinski, R., & Blochtein, B. (2014). Diapause in Stingless Bees (Hymenoptera: Apidae). Sociobiology, 61(4), 369–377. https://doi.org/10.13102/sociobiology.v61i4.369-377




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