Environmental windows for foraging activity in stingless bees, Melipona subnitida Ducke and Melipona quadrifasciata Lepeletier (Hymenoptera: Apidae: Meliponini)
Keywords:Meliponini, pollen foraging, thermal window, resource overlap, colony survival
The foraging success of a bee species is limited to an environmental window, a combination of optimal ambient temperatures and resource availability. Mismatches between flowering and optimal foraging temperature may lead to a reduction of a colony's food intake and, eventually, of brood production. In the present study, we evaluated the pollen foraging activity of two native Brazilian meliponine species Melipona quadrifasciata and M. subnitida at the campus of the University of São Paulo at Ribeirão Preto (March, 2010 – January, 2011). Whereas M. quadrifasciata naturally occurs in the study region (Brazilian Southeast), M. subnitida is restricted to the Brazilian Northeast. This difference in geographic distribution and concordant climatic specializations suggest differences concerning the environmental window between the two species. We investigated potential differences between the species concerning the thermal window within which foraging occurs, and consequent differences in foraging activity, visited pollen sources, and colony survival. The lower temperature limit for M. subnitida (17 ºC) was 5 °C above the lower temperature limit found in M. quadrifasciata (12 °C). This difference resulted in a considerable time lag concerning the onset of foraging between the bee species (maximum: 120 minutes), mainly so in the cold/dry season. Due to this delay in foraging, M. subnitida could benefit from highly profitable pollen sources (mass-flowering trees) that were in bloom during this time of the year. Possibly in consequence of this deficit in pollen intake, three of the six monitored colonies of M. subnitida did not survive the study period.
Aleixo, K.P., Faria, L.B., Garófalo, C.A., Fonseca, V.L.I., & Silva, C.I. (2013). Pollen collected and foraging activities of Frieseomelitta varia (Lepeletier) (Hymenoptera: Apidae) in an urban landscape. Sociobiology, 60: 266-276.
Aleixo, K.P., Faria, L.B., Groppo, M., Nascimento Castro M.M. & Silva. C.I. (2014). Spatiotemporal distribution of floral resources in a Brazilian city: Implications for the maintenance of pollinators, especially bees. Urban For. Urban Gree., http://dx.doi.org/10.1016/j.ufug.2014.08.002.
Bawa, K.S. (1983). Patterns of flowering in tropical plants. In: C.E. Jones & R.J. Little (Eds.), Handbook of Experimental Pollination Biology (pp. 394-410). New York: Van Nostrand Reinhold.
Biesmeijer, J.C., Smeets, M.J.A.P., Richter, J.A.P. & Sommeijer, M.J. (1999). Nectar foraging by stingless bees in Costa Rica: botanical and climatological influences on sugar concentration of nectar collected by Melipona. Apidologie, 30: 43-55.
Buchmann, S.L. (1983). Buzz pollination in angiosperms. In: C.E. Jones & R.J. Little (Eds.), Handbook of Experimental Pollination Biology (pp. 73-113). New York: Van Nostrand Reinhold.
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. http://www.moure.cria.org.br/catalogue.
Eltz, T., Brühl, C.A. van der Kaars, S., Chey, V.K. & Linsenmair, K.E. (2001). Pollen foraging and resource partitioning of stingless bees in relation to flowering dynamics in a Southeast Asian tropical rainforest. Insect. Soc., 48: 273-279.
Erdtman, G. (1960). The acetolized method - a revised description. Sven. Bot. Tidskr., 54: 561-564.
Faria, L.B., Aleixo, K.P., Garófalo, C.A., Imperatriz-Fonseca, V.L. & Silva, C.I. (2012). Foraging of Scaptotrigona aff. depilis (Hymenoptera, Apidae) in an urbanized area: Seasonality in resource availability and visited plants. Psyche, 2012: 2012, Article ID 630628, doi: 10.1155/2012/630628.
Ferreira-Junior, N.T., Blochtein, B. & Moraes, J.F. (2010). Seasonal flight and resource collection patterns of colonies of the stingless bee Melipona bicolor schencki Gribodo (Apidae, Meliponini) in an Araucaria forest. Rev. Bras. Entomol., 54: 630-636.
Gentry, A. (1974). Flowering phenology and diversity in tropical Bignoniaceae. Biotropica 6: 64-68.
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. Ecol. Model., 244: 127-131.
Guisan, A. & Thuiller, W. (2005). Predicting species distribution: offering more than simple habitat models. Ecol. Lett., 8: 993-1009.
Hegland, S. J., Nielsen, A., Lázaro, A., Bjerknes, A.L. & Totland, Ø. (2009). How does climate warming affect plant-pollinator interactions? Ecol. Lett., 12: 184-195.
Heinrich, B. (1993). The Hot-Blooded Insects: Strategies and Mechanisms of Thermoregulation. Berlin: Springer-Verlag.
Hilário, S.D., Imperatriz-Fonseca, V.L., & Kleinert, A.M.P. (2000). Flight activity and colony strength in the stingless bee Melipona bicolor bicolor (Apidae, Meliponinae). Rev. Bras. Biol., 60: 299-306.
Hrncir, M. & Maia-Silva, C. (2013). On the diversity of foraging-related traits in stingless bees. In: P. Vit, P., S.R.M. Pedro & Roubik, D. (Eds.), Pot-Honey: A Legacy of Stingless Bees (pp. 201–215). New York: Springer.
Imperatriz-Fonseca, V.L. Canhos, D.A.L., Alves, D.A. & Saraiva, A.M. (2012). Polinizadores no Brasil - Contribuição e Perspectivas para a Biodiversidade, Uso Sustentável, Conservação e Serviços Ambientais. São Paulo: EDUSP.
Koedam, D., Contrera, F.A.L. & Imperatriz-Fonseca, V.L. (1999). Clustered male production by workers in the stingless bee Melipona subnitida Ducke (Apidae, Meliponinae). Insect. Soc., 46: 387-391.
Maia-Silva, C. (2013). Adaptações comportamentais de Melipona subnitida (Apidae, Meliponini) às condições ambientais do semiárido brasileiro. Doctoral thesis. Universidade de São Paulo, Ribeirão Preto.
Marengo, J.A., Jones R., Alves L.M. & Valverde M.C. (2009). Future change of temperature and precipitation extremes in South America as derived from the PRECIS regional climate modelling system. Int. J. Climatol., 29: 2241-2255.
Memmott, J., Craze, P.G., Waser, N.M. & Price, M.V. (2007). Global warming and the disruption of plant-pollinator interactions. Ecol. Lett., 10: 710-717.
Michener, C.D. (1974). The Social Behavior of the Bees: a Comparative Study. Cambridge: Harvard University Press.
Michener, C.D. (2000). The Bees of the World. Baltimore: The Johns Hopkins University Press.
Nagamitsu, T., Momose, K., Inoue, T. & Roubik, D.W. (1999). Preference in flower visits and partitioning in pollen diets of stingless bees in an Asian tropical rain forest. Res. Popul. Ecol., 41: 195-202.
Nobre, P. (2011). Mudanças climáticas e desertificação: os desafios para o Estado Brasileiro. In: R.C.C. Lima, A.M.B. Cavalcante & A.M.P. Marin (Eds.), Desertificação e Mudanças Climáticas no Semiárido Brasileiro (pp. 25-35). Campina Grande: Instituto Nacional do Semiárido.
Nogueira-Neto, P. (1997). Vida e Criação de Abelhas Indígenas Sem Ferrão. São Paulo: Editora Nogueirapis.
Oliveira, R.C., Menezes, C., Soares, A.E.E. & Imperatriz- Fonseca, V.L. (2013). Trap-nests for stingless bees (Hymenoptera, Meliponini). Apidologie, 44: 29-37.
Pais, M. & Varanda, E.M. (2010). Arthropod recolonization in the restorarion of a semideciduous forest in southeastern Brazil. Neotrop. Entomol., 39: 198-206.
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.
Prado, D. (2003). As Caatingas da América do Sul. In: I.R. Leal, M. Tabarelli & J.M.C. Silva (Eds.), Ecologia e Conservação da Caatinga (pp. 75-134). Recife: Editora Universitária UFPE.
Proença, C. & Gibbs, P. E. (1994). Reproductive biology of eight sympatric Myrtaceae from Central Brazil. New Phytol. 126: 343-354.
Ramalho, M. (2004). Stingless bees and mass flowering trees in the canopy of Atlantic Forest: a tight relationship. Acta Bot. Bras. 18: 37-47.
Ribeiro, M.F., Imperatriz-Fonseca, V.L. & Santos Filho, P.S. (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.
Sánches-Azofeita, A., Powers, J.S., Fernandes, G.W. & Quesada, M. (2013). Tropical Dry Forests in the Americas: Ecology, Conservation, and Management. Boca Raton: CRC Press.
Schwarz, H.F. (1932). The genus Melipona - the type genus of the Meliponidae or stingless bees. B. Am. Mus. Nat. Hist., 63: 231-460.
Silva, A.L.G. & Pinheiro, M.C.B. (2007). Biologia floral e da polinização de quatro espécies de Eugenia L. (Myrtaceae). Acta Bot. Bras., 21: 235-247.
Stone, G.N. (1993). Endothermy in the solitary bee Anthophora plumipes: independent measures of thermoregulatory ability, costs of warm-up and the role of body size. J. Exp. Biol., 174: 299-320.
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. Ecol. Entomol., 24: 208–221.
Wilms, W. Imperatriz-Fonseca, V. L. & Engels, W. (1996). Resource partitioning between highly eusocial bees and possible impact of the introduced Africanized honey bee on native stingless bees in the Brazilian Atlantic. Stud. Neotrop. Fauna Environ., 31: 137-151.
Zanella, F. (2000). The bees of the Caatinga (Hymenoptera, Apoidea, Apiformes): a species list and comparative notes regarding their distribution. Apidologie, 31: 579-592.
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