Keywords:
foraging
nectar
pollen
maya bees
honey bees

  • Abstract

    The Maya bee, Melipona beecheii, has been an integral part of Mayan culture on the Yucatan Peninsula for several centuries. In the present study, we explore the daily food-foraging behavior of M. beecheii during the year and compare its foraging behavior during summer and winter with the foraging behavior of honeybees during the same periods in the Yucatan Peninsula. Annual behavior showed a remarkable tendency toward pollen foraging during the early hours of the day, whereas nectar foraging peaked at midday. Factors such as season, resource, and hour significantly influence the daily activity of M. beecheii and A. mellifera. We detected noticeable differences in foraging behavior between summer and winter in both Maya bees and honeybees. Honeybees preferred foraging earlier pollen during winter and nectar during summer, whereas Maya bees preferred foraging pollen earlier during summer. Finally, we observed that both bee species made far more foraging trips during winter than in summer.

  • References

    1. Abrol, D. P. (2006). Foraging behaviour of bees as influenced by quality and quantity of rewards from flowers. Journal of Asia-Pacific Entomology, 9(2), 145–148. https://doi.org/10.1016/S1226-8615(08)60285-X
    2. Aleixo, K. P., Menezes, C., Imperatriz-Fonseca, V. L., & da Silva, C. I. (2017). Seasonal availability of floral resources and ambient temperature shape stingless bee foraging behavior (Scaptotrigona aff. depilis). Apidologie, 48, 117–127.
    3. Alves, D. D. A., Imperatriz-Fonseca, V. L., & Santos-Filho, P. D. 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.
    4. Balfour, N. J., Gandy, S., & Ratnieks, F. L. (2015). Exploitative competition alters bee foraging and flower choice. Behavioral Ecology and Sociobiology, 69, 1731–1738.
    5. Batista, M. D. C. S., Pessoa, R. M. S., Gois, G. C., Silva, A. A. F., Lima, C. A. B., & Cunha, D. S. (2018). Alimentação das abelhas: Revisão sobre a flora apícola e necessidades nutricionais. Journal of Biology and Pharmacy, 14, 62–72. https://revista.uepb.edu.br/BIOFARM/article/view/2105
    6. Biesmeijer, J. C., van Nieuwstadt, M. G., 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.
    7. Biesmeijer, J. C., Richter, J. A., Smeets, M. A., & Sommeijer, M. J. (1999). Niche differentiation in nectar‐collecting stingless bees: The influence of morphology, floral choice and interference competition. Ecological Entomology, 24, 380–388. https://doi.org/10.1046/j.1365-2311.1999.00220.x
    8. Biesmeijer, J. C., van Nieuwstadt, M. V., Sommeijer, M. J., & de Bruijn, L. D. (1994). Pollen foraging strategies of two domesticated stingless bee species in Costa Rica. Apidologie, 25, 209–224.
    9. 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, 23, 711–715. https://doi.org/10.1590/S0101-81752006000300015
    10. Cairns, C. E., Villanueva‐Gutiérrez, R., Koptur, S., & Bray, D. B. (2005). Bee populations, forest disturbance, and Africanization in Mexico. Biotropica: The Journal of Biology and Conservation, 37, 686–692. https://doi.org/10.1111/j.1744-7429.2005.00087.x
    11. Carvalho-Zilse, G. A., Porto, E. L., Silva, C. G., & Costa Pinto, M. D. (2007). Atividades de vôo de operárias de Melipona seminigra (Hymenoptera: Apidae) em um sistema agroflorestal da Amazônia. Bioscience Journal, 23, 94–99.
    12. Chouvalova, A., & Limeri, L. (2023). Niches and competition. In Introductory Biology 2. Texas Tech University.
    13. Corbet, S. A. (2003). Nectar sugar content: Estimating standing crop and secretion rate in the field. Apidologie, 34, 1–10. https://doi.org/10.1051/apido:2002049
    14. Dafni, A., & Shmida, A. (1996). The possible ecological implications of the invasion of Bombus terrestris. In A. Matheson, S. L. Buchmann, C. O’Toole, P. Westrich, & I. H. Williams (Eds.), The Conservation of Bees (pp. 183–200). Academic Press.
    15. De Bruijn, L. L. M., & Sommeijer, M. J. (1997). Colony foraging in different species of stingless bees (Apidae, Meliponinae) and the regulation of individual nectar foraging. Insectes Sociaux, 44, 35–47.
    16. Deppe, J. L., Dress, W. J., Nastase, A. J., Newell, S. J., & Luciano, C. S. (2000). Diel variation of sugar amount in nectar from pitchers of Sarracenia purpurea L. with and without insect visitors. The American Midland Naturalist, 144, 123–132. https://doi.org/10.1674/0003-0031(2000)144[0123:DVOSAI]2.0.CO;2
    17. Di Trani, J. C., & Villanueva-Gutiérrez, R. (2018). Annual foraging patterns of the Maya bee Melipona beecheii (Bennett, 1831). In Pot-Pollen in Stingless Bee Melittology (pp. 131–138).
    18. Di Trani, J. C., Ramírez, V. M., Añino, Y., & Barba, A. (2022). Environmental conditions and bee foraging on watermelon crops in Panama. Journal of Animal Behaviour and Biometeorology, 10, Article 2234. https://10.31893/jabb.22034
    19. Dos Santos, C. F., Nunes-Silva, P., Halinski, R., & Blochtein, B. (2015). Diapause in stingless bees (Hymenoptera: Apidae). Sociobiology, 61, 369–377.
    20. Echazarreta, C. M., & Paxton, R. J. (1997). Comparative colony development of Africanized and European honey bees (Apis mellifera) in lowland neotropical Yucatan, Mexico. Journal of Apicultural Research, 36, 89–103. https://doi.org/10.1080/00218839.1997.11100934
    21. Eckert, C. D. (1990). The relationship between colony state and individual foraging behavior in the honey bee, Apis mellifera L. (Master’s thesis). Simon Fraser University, Burnaby, BC, Canada.
    22. Engels, W., Rosenkranz, P., & Engels, E. (1995). Thermoregulation in the nest of the Neotropical stingless bee Scaptotrigona postica and a hypothesis on the evolution of temperature homeostasis in highly eusocial bees. Studies on Neotropical Fauna and Environment, 30(3), 193–205. https://doi.org/10.1080/01650529509360958
    23. Fidalgo, A. D. O., & Kleinert, A. D. M. P. (2007). Foraging behavior of Melipona rufiventris Lepeletier (Apinae; Meliponini) in Ubatuba, SP, Brazil. Brazilian Journal of Biology, 67(1), 133–140. https://doi.org/10.1590/S1519-69842007000100018
    24. Fletcher, D. J. C., & Crewe, R. M. (1981). Nest structure and thermoregulation in the stingless bee Trigona (Plebeina) denoiti Vachal (Hymenoptera: Apidae). Journal of the Entomological Society of Southern Africa, 44(2), 183–196.
    25. Fowler, R. E., Rotheray, E. L., & Goulson, D. (2016). Floral abundance and resource quality influence pollinator choice. Insect Conservation and Diversity, 9(6), 481–494. https://doi.org/10.1111/icad.12197
    26. Freitas, X. F. P. V. D., da Silva, I. E., Faquinello, P., Zanata, R. A., Arnhold, E., & Silva-Neto, C. D. M. (2022). External activity of the stingless bee Melipona fasciculata (Smith) kept in the Brazilian Cerrado. Journal of Apicultural Research, 61(3), 429–434. https://doi.org/10.1080/00218839.2020.1745436
    27. Gobatto, A. L., & Knoll, F. (2013). Influence of seasonal changes in daily activity and annual life cycle of Geotrigona mombuca (Hymenoptera, Apidae) in a Cerrado habitat, São Paulo, Brazil. Iheringia. Série Zoologia, 103(4), 367–373. https://doi.org/10.1590/S0073-47212013000400006
    28. Goulson, D. (2003). Effects of introduced bees on native ecosystems. Annual Review of Ecology, Evolution, and Systematics, 34, 1–26. https://doi.org/10.1146/annurev.ecolsys.34.011802.132355
    29. Gouw, M. S., & Gimenes, M. (2013). Differences of the daily flight activity rhythm in two neotropical stingless bees (Hymenoptera, Apidae). Sociobiology, 60(2), 183–189. https://doi.org/10.13102/sociobiology.v60i2.183-189
    30. Guibu, L. S., & Imperatriz-Fonseca, V. L. (1984). Atividade externa de Melipona quadrifasciata Lepeletier (Hymenoptera, Apidae, Meliponinae). Ciência e Cultura, 36, 623.
    31. Heard, T. A., & Hendrikz, J. K. (1993). Factors influencing flight activity of colonies of the stingless bee Trigona carbonaria (Hymenoptera, Apidae). Australian Journal of Zoology, 41(4), 343–353. https://doi.org/10.1071/ZO9930343
    32. Hepburn, H. R., Pirk, C. W. W., & Duangphakdee, O. (2014). Honeybee nests: Composition, structure, function. Springer.
    33. Hilário, S. D., Imperatriz-Fonseca, V. L., & Kleinert, A. (2000). Flight activity and colony strength in the stingless bee Melipona bicolor bicolor (Apidae, Meliponinae). Revista Brasileira de Biologia, 60(2), 299–306. https://doi.org/10.1590/S0034-71082000000200014
    34. Hilário, S. D., Ribeiro, M. D. F., & Imperatriz-Fonseca, V. L. (2007). Impacto da precipitação pluviométrica sobre a atividade de vôo de Plebeia remota (Holmberg, 1903) (Apidae, Meliponini). Biota Neotropica, 7(1), 135–143. https://doi.org/10.1590/S1676-06032007000300016
    35. Inoue, T., Salmah, S., Abbas, I., & Yusuf, E. (1985). Foraging behavior of individual workers and foraging dynamics of colonies of three Sumatran stingless bees. Researches on Population Ecology, 27(2), 373–392.
    36. Inouye, D. W. (1978). Resource partitioning in bumblebees: Experimental studies of foraging behavior. Ecology, 59(4), 672–678. https://doi.org/10.2307/1938769
    37. Iwama, S. (1977). A influência de fatores climáticos na atividade externa de Tetragonisca angustula (Apidae, Meliponinae). Boletim de Zoologia da Universidade de São Paulo, 2, 189–201.
    38. Jensen, A. L. (1987). Simple models for exploitative and interference competition. Ecological Modelling, 35(2), 113–121. https://doi.org/10.1016/0304-3800(87)90093-7
    39. Jha, S., & Vandermeer, J. H. (2009). Contrasting foraging patterns for Africanized honeybees, native bees and native wasps in a tropical agroforestry landscape. Journal of Tropical Ecology, 25(1), 13–22. https://doi.org/10.1017/S026646740800566X
    40. Johnson, L. K., & Hubbell, S. P. (1974). Aggression and competition among stingless bees: Field studies. Ecology, 55(1), 120–127. https://doi.org/10.2307/1934624
    41. Jones, J. C., & Oldroyd, B. P. (2006). Nest thermoregulation in social insects. Advances in Insect Physiology, 33, 153–191. https://doi.org/10.1016/S0065-2806(06)33003-2
    42. Juliani, L. (1967). A descrição do ninho e alguns dados biológicos sobre a abelha Plebeia julianii Moure 1962 (Hymenoptera, Apidae). Revista Brasileira de Entomologia, 12, 1–58.
    43. Kajobe, R., & Echazarreta, C. M. (2005). Temporal resource partitioning and climatological influences on colony flight and foraging of stingless bees (Apidae; Meliponini) in Ugandan tropical forests. African Journal of Ecology, 43, 267–275. https://doi.org/10.1111/j.1365-2028.2005.00586.x
    44. Kleinert-Giovannini, A., & Imperatriz-Fonseca, V. L. (1986). Flight activity and responses to climatic conditions of two subspecies of Melipona marginata Lepeletier (Apidae, Meliponinae). Journal of Apicultural Research, 25, 3–8. https://doi.org/10.1080/00218839.1986.11100685
    45. Leal-Ramos, A., & León-Sánchez, L. E. (2013). Antagonism of Apis mellifera and Melipona beecheii for the sources of feeding. Revista Cubana de Ciencias Forestales, 1, 102–109.
    46. Macías-Macías, J. O., Quezada-Euán, J. J. G., Contreras-Escareño, F., Tapia-Gonzalez, J. M., Moo-Valle, H., & Ayala, R. (2011). Comparative temperature tolerance in stingless bee species from tropical highlands and lowlands of Mexico and implications for their conservation (Hymenoptera: Apidae: Meliponini). Apidologie, 42, 679–689.
    47. Michener, C. D. (1974). The social behavior of the bees: A comparative study. Harvard University Press.
    48. Michener, C. D. (2000). The bees of the world. JHU Press.
    49. Nagamitsu, T., & Inoue, T. (1997). Aggressive foraging of social bees as a mechanism of floral resource partitioning in an Asian tropical rainforest. Oecologia, 110, 432–439.
    50. Nascimento, D. L., & Nascimento, F. S. (2012). Extreme effects of season on the foraging activities and colony productivity of a stingless bee (Melipona asilvai Moure, 1971) in Northeast Brazil. Psyche: A Journal of Entomology, 2012, 267361. https://doi.org/10.1155/2012/267361
    51. Nicolson, S. W., De Veer, L., Köhler, A., & Pirk, C. W. (2013). Honeybees prefer warmer nectar and less viscous nectar, regardless of sugar concentration. Proceedings of the Royal Society B: Biological Sciences, 280, 20131597. https://doi.org/10.1098/rspb.2013.1597
    52. Nogueira-Neto, P. (1997). Vida e criação de abelhas indígenas sem ferrão. Ed. Nogueirapis.
    53. Nunes-Silva, P., Hilário, S. D., Santos Filho, P. D. 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, 2010, 241204. https://doi.org/10.1155/2010/241204
    54. Ogilvie, J. E., & Forrest, J. R. (2017). Interactions between bee foraging and floral resource phenology shape bee populations and communities. Current Opinion in Insect Science, 21, 75–82. https://doi.org/10.1016/j.cois.2017.05.015
    55. Oliveira, F. L. D., Dias, V. H. P., Costa, E. M. D., Filgueira, M. A., & Espínola Sobrinho, J. (2012). Influência das variações climáticas na atividade de vôo das abelhas jandairas Melipona subnitida Ducke (Meliponinae). Revista Ciência Agronômica, 43, 598–603. https://doi.org/10.1590/S1806-66902012000300024
    56. Oliveira-Abreu, C., Hilário, S. D., Luz, C. F. P., & dos Santos, I. A. (2014). Pollen and nectar foraging by Melipona quadrifasciata anthidioides Lepeletier (Hymenoptera: Apidae: Meliponini) in natural habitat. Sociobiology, 61, 441–448. https://doi.org/10.13102/sociobiology.v61i4.441-448
    57. Pat-Fernández, L. A., Anguebes Franceschi, F., Pat Fernández, J. M., Hernández Bahena, P., & Ramos Reyes, R. (2018). Condición y perspectivas de la meliponicultura en comunidades mayas de la reserva de la biósfera Los Petenes, Campeche, México. Estudios de Cultura Maya, 52, 227–254. https://doi.org/10.19130/iifl.ecm.2018.52.939
    58. Pereboom, J. J. M., & Biesmeijer, J. C. (2003). Thermal constraints for stingless bee foragers: The importance of body size and coloration. Oecologia, 137, 42–50.
    59. 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. https://doi.org/10.1590/S0101-81752003000400001
    60. Polatto, L. P., Chaud-Netto, J., & Alves-Junior, V. V. (2014). Influence of abiotic factors and floral resource availability on daily foraging activity of bees: Influence of abiotic and biotic factors on bees. Journal of Insect Behavior, 27, 593–612.
    61. Quezada-Euán, J. J. G., de Jesús May-Itzá, W., & González-Acereto, J. A. (2001). Meliponiculture in Mexico: Problems and perspective for development. Bee World, 82, 160–167. https://doi.org/10.1080/0005772X.2001.11099523
    62. Reyes-González, A., & Zamudio, F. (2020). Competition interactions among stingless bees (Apidae: Meliponini) for Croton yucatanensis Lundell resins. International Journal of Tropical Insect Science, 40, 1099–1104.
    63. Roubik, D. W. (1980). Foraging behavior of competing Africanized honeybees and stingless bees. Ecology, 61, 836–845. https://doi.org/10.2307/1936754
    64. Roubik, D. W. (1989). Ecology and natural history of tropical bees. Cambridge University Press.
    65. Roubik, D. W. (2009). Ecological impact on native bees by the invasive Africanized honey bee. Acta Biológica Colombiana, 14, 15–24.
    66. Schaffer, W. M., Jensen, D. B., Hobbs, D. E., Gurevitch, J., Todd, J. R., & Schaffer, M. V. (1979). Competition, foraging energetics, and the cost of sociality in three species of bees. Ecology, 60, 976–987. https://doi.org/10.2307/1936866
    67. Secretaría de Desarrollo Agrario, Territorial y Urbano – SEDATU. (2024). Programa de Desarrollo Urbano de Chetumal-Calderitas-Subteniente López-Huay-Pix y Xul-Há. Municipio de Othón P. Blanco, Estado de Quintana Roo. H. Ayuntamiento de Othón P. Blanco. https://www.opb.gob.mx/portal/wp-content/uploads/transparencia/93/I/f/PDU2018/PDU%20integrado%2019012018-publicacion%20digital.pdf
    68. Slaa, E. J., Tack, A. J., & Sommeijer, M. J. (2003). The effect of intrinsic and extrinsic factors on flower constancy in stingless bees. Apidologie, 34, 457–468. https://doi.org/10.1051/apido:2003046
    69. Souza-Junior, J. B. F., de Queiroz, J. P. A. F., & de Sousa Linhares, C. M. (2020). Influence of the thermal environment on the stingless bee foraging activity: A mini-review. Journal of Animal Behaviour and Biometeorology, 7, 176–178.
    70. Stone, G. N., Gilbert, F., Willmer, P., Potts, S., Semida, F., & Zalat, S. (1999). Windows of opportunity and the temporal structuring of foraging activity in a desert solitary bee. Ecological Entomology, 24, 208–221. https://doi.org/10.1046/j.1365-2311.1999.00181.x
    71. Streinzer, M., Huber, W., & Spaethe, J. (2016). Body size limits dim-light foraging activity in stingless bees (Apidae: Meliponini). Journal of Comparative Physiology A, 202, 643–655.
    72. Tepedino, V., Horn, L. A., & Durham, S. (2016). Pollen removal and deposition by pollen- and nectar-collecting specialist and generalist bee visitors to Iliamna bakeri (Malvaceae). Journal of Pollination Ecology, 19, 50–56. https://doi.org/10.26786/1920-7603(2016)2
    73. Teixeira, L. V., & Campos, F. D. N. M. (2005). Início da atividade de vôo em abelhas sem ferrão (Hymenoptera, Apidae): Influência do tamanho da abelha e da temperatura ambiente. Revista Brasileira de Zoociências, 7, 195–202.
    74. Thomson, D. (2004). Competitive interactions between the invasive European honey bee and native bumble bees. Ecology, 85, 458–470. https://doi.org/10.1890/02-0626
    75. Van Veen, J. W., & Arce Arce, H. G. (1999). Nest and colony characteristics of log-hived Melipona beecheii (Apidae: Meliponinae). Journal of Apicultural Research, 38, 43–48. https://doi.org/10.1080/00218839.1999.11100994
    76. Vijayan, M., Saravanan, P. A., & Srinivasan, M. R. (2018). Effect of season and timings on the foraging behaviour of stingless bee, Tetragonula iridipennis Smith (Hymenoptera: Apidae). Madras Agricultural Journal, 105, 286–290.
    77. Villanueva-Gutiérrez, R., Roubik, D. W., & Colli-Ucán, W. (2005). Extinction of Melipona beecheii and traditional beekeeping in the Yucatán peninsula. Bee World, 86, 35–41. https://doi.org/10.1080/0005772X.2005.11099651
    78. Villanueva-Gutiérrez, R., Roubik, D. W., Colli-Ucán, W., Güemez-Ricalde, F. J., & Buchmann, S. L. (2013a). A critical view of colony losses in managed Mayan honey-making bees (Apidae: Meliponini) in the heart of Zona Maya. Journal of the Kansas Entomological Society, 86, 352–362. https://doi.org/10.2317/JKES130131.1
    79. Villanueva-Gutiérrez, R., Colli-Ucán, W., Novelo, M. T., & Gracia, M. A. (2013b). Recuperación de saberes y formación para el manejo y conservación de la abeja Melipona beecheii en la Zona Maya de Quintana Roo, México. In P. Vit & D. W. Roubik (Eds.), Stingless bees process honey and pollen in cerumen pots (pp. 1–8).
    80. Villanueva-Gutiérrez, R., Roubik, D. W., & Porter-Bolland, L. (2015). Bee–plant interactions: Competition and phenology of flowers visited by bees. In Biodiversity and conservation of the Yucatán Peninsula (pp. 131–152).
    81. Vossler, F. G., Tellería, M. C., & Cunningham, M. (2010). Floral resources foraged by Geotrigona argentina (Apidae, Meliponini) in the Argentine Dry Chaco forest. Grana, 49(2), 142–153. https://doi.org/10.1080/00173131003694274
    82. Willmer, P. G. (1983). Thermal constraints on activity patterns in nectar-feeding insects. Ecological Entomology, 8(4), 455–469.
    83. Willmer, P. G. (2011). Pollination and floral ecology. Princeton University Press. https://doi.org/10.1515/9781400838943
    84. Willmer, P. G. (1991). Constraints on foraging by solitary bees. In L. J. Goodman & R. C. Fisher (Eds.), The behaviour and physiology of bees (pp. 131–148).
    85. Willmer, P. G., & Stone, G. N. (2004). Behavioral, ecological, and physiological determinants of the activity patterns of bees. Advances in the Study of Behavior, 34, 347–466.
    86. Winston, M. L. (1980). Seasonal patterns of brood rearing and worker longevity in colonies of the Africanized honey bee (Hymenoptera: Apidae) in South America. Journal of the Kansas Entomological Society, 53(1), 157–165.
    87. Winston, M. L. (1987). The biology of the honey bee. Harvard University Press.
    88. Wojcik, V. A., Morandin, L. A., Davies Adams, L., & Rourke, K. E. (2018). Floral resource competition between honey bees and wild bees: Is there clear evidence and can we guide management and conservation? Environmental Entomology, 47(4), 822–833. https://doi.org/10.1093/ee/nvy077
    89. Yokoi, T., & Fujisaki, K. (2011). To forage or not: Responses of bees to the presence of other bees on flowers. Annals of the Entomological Society of America, 104(2), 353–357. https://doi.org/10.1603/AN10053
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Trani, J. C. D., & Añino, Y. (2025). Daily foraging activity of the Maya bee (<em>Melipona beecheii</em>) in Chetumal, México. Journal of Animal Behaviour and Biometeorology, 13(1), 2025009. https://doi.org/10.31893/jabb.2025009
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