Abstract
In stingless bees (Meliponini) like in many other eusocial insect colonies food hoarding plays an important role in colony survival. However, very little is known on how Meliponini, a taxon restricted to tropical and subtropical regions, respond to different store conditions. We studied the impact of honey removal on nectar foraging activity and recruitment behaviour in Melipona scutellaris and compared our results with studies of the honey bee Apis mellifera. As expected, foraging activity increased significantly during abundance of artificial nectar and when increasing its profitability. Foraging activity on colony level could thereby frequently increase by an order of magnitude. Intriguingly, however, poor honey store conditions did not induce increased nectar foraging or recruitment activity. We discuss possible reasons explaining why increasing recruitment and foraging activity are not used by meliponines to compensate for poor food conditions in the nest. Among these are meliponine specific adaptations to climatic and environmental conditions, as well as physiology and brood rearing, such as mass provisioning of the brood.
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References
Alves RM, Carvalho CA, Souza BA, Santos WS (2012) Areas of natural occurrence of Melipona scutellaris Latreille, 1811 (Hymenoptera: apidae) in the State of Bahia, Brazil. An Acad Bras Cienc 84:679–688
Barth FG, Hrncir M, Jarau S (2008) Signals and cues in the recruitment behavior of stingless bees (Meliponini). J Comp Physiol A 194:313–327
Batista MA, Ramalho M, Soares AE (2003) Nesting sites and abundance of Meliponini (Hymenoptera: apidae) in heterogeneous habitats of the Atlantic rain forest, Bahia, Brazil. Lundiana 4:19–23
Camargo JMF (2013) Historical biogeography of the Meliponini (Hymenoptera, Apidae, Apinae) of the Neotropical Region. In: Vit P, Pedro SRM, Roubik D (eds) Pot-honey: a legacy of stingless bees. Springer, New York, pp 3–17
Cartar RV (1992) Adjustment of foraging effort and task switching in energy-manipulated wild bumblebee colonies. Anim Behav 44:75–87
Crailsheim K (1990) The protein balance of the honey bee worker. Apidologie 21:417–429
Crailsheim K, Schneider LHW, Hrassnigg N, Bühlmann G, Brosch U, Gmeinbauer R, Schöffmann B (1992) Pollen consumption and utilisation in worker honey bees: dependence on individual age and function. J Insect Physiol 38:409–419
Crailsheim K, Hrassnigg N, Gmeinbauer R, Szolderits M, Schneider LHW, Brosch U (1993) A comparison of pollen consumption and digestion in non-breeding honeybees in winter. J Insect Physiol 39:369–373
Dornhaus A (2002) The role of communication in the foraging process of social bees. Doctoral dissertation, University of Würzburg, Würzburg, Germany
Edgington S (1995) Randomization tests, 3rd edn. Marcel Dekker, New York
Free JB, Williams I (1972) Hoarding by honeybees (Apis mellifera L.). Anim Behav 20:327–334
Gordon DM (1996) The organization of work in social insect colonies. Nature 380:121–124
Hrassnigg N, Brodschneider R, Fleischmann P, Crailsheim K (2003) Honeybee drones are not able to utilize starch as fuel for flight but worker bees (Apis mellifera L.) are able to. In: 38th Apimondia Congress, Ljubljana, Slovenia
Hrncir M (2009) Mobilizing the foraging force - mechanical signals in stingless bee recruitment. In: Jarau S, Hrncir M (eds) Food exploitation by social insects: ecological, behavioral, and theoretical approaches. CRC Press, Boca Raton, pp 199–221
Hrncir M, Barth FG (2014) Vibratory communication in stingless bees (Meliponini): the challenge of interpreting the signals. In: Cocroft RB, Gogala M, Hill PSM, Wessel A (eds) Studying vibrational communication. Springer, Berlin Heidelberg, pp 349–374
Hrncir M, Jarau S, Zucchi R, Barth FG (2004a) On the origin and properties of scent marks deposited at the food source by a stingless bee, Melipona seminigra. Apidologie 35:3–13
Hrncir M, Jarau S, Zucchi R, Barth FG (2004b) Thorax vibrations of a stingless bee (Melipona seminigra) II. Dependence on sugar concentration. J Comp Physiol A 190:549–560
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 Press, Boca Raton, pp 223–249
Jarau S, Hrncir M, Zucchi R, Barth FG (2000) Recruitment behavior in stingless bees, Melipona scutellaris and Melipona quadrifasciata I. Foraging at food sources differing in direction and distance. Apidologie 31:81–91
Jarau S, Hrncir M, Schmidt VM, Zucchi R, Barth FG (2003) Effectiveness of recruitment behavior in stingless bees (Apidae, Meliponini). Insect Soc 50:365–374
Jones JC, Oldroyd BP (2007) Nest thermoregulation in social insects. Adv Insect Physiol 33:153–191
Kerr WE, Carvalho GA, Nascimento VA (1996) Abelha uruçu: biologia, manejo e conservação. Fundação Acangaú, Paracatu
Kugler H (1943) Hummeln als Blütenbesucher. Erg biol 19:143–323
Lichtenberg EM, Zivin JG, Hrncir M, Nieh JC (2014) Eavesdropping selects for conspicuous signals. Curr Biol 24:R598–R599
Lindauer M (1948) Über die Einwirkung von Duft und Geschmackstoffen sowie anderer Faktoren auf die Tänze der Bienen. Z vergl Physiol 31:348–412
Lindauer M (1952) Ein Beitrag zur Frage der Arbeitsteilung im Bienenstaat. Z vergl Physiol 34:299–345
Lindauer M (1954) Temperaturregulierung und Wasserhaushalt im Bienenstaat. Z vergl Physiol 36:391–432
Lindauer M (1956) Über die Verständigung bei indischen Bienen. Z vergl Physiol 38:521–557
Lindauer M, Kerr WE (1958) Die gegenseitige Verständigung bei den stachellosen Bienen. Z vergl Physiol 41:405–434
Maia-Silva C, Hrncir M, Silva CI, Imperatriz-Fonseca VL (2015) Survival strategies of stingless bees (Melipona subnitida) in an unpredictable environment, the Brazilian tropical dry forest. Apidologie 46:631–643
Maia-Silva C, Hrncir M, Imperatriz-Fonseca VL, Schorkopf DLP (2016) Stingless bees (Melipona subnitida) adjust brood production rather than foraging activity in response to changes in pollen stores. J Comp Physiol A. doi:10.1007/s00359-016-1095-y
Manly BJF (1997) Randomization, bootstrap and Monte Carlo methods in biology. Chapman and Hall, London
Martinho MR (1975a) Contribuição ao estudo da digestão do grão de pólen em Melipona quadrifasciata anthidioides Lepeltier (Hymenoptera, Apidae, Meliponinae). Masters study. University of São Paulo, Ribeirão Preto, São Paulo
Martinho MR (1975b) Contribution to the study of the digestion of pollen grains in the Melipona cuadrifasciata anthidioides Lepeltier (Hymenoptera, Apidae, Meliponinae). The bee and the environment (The XXVth International Apicultural Congress of Apimondia in Grenoble, France). Apimondia Publishing House, Bucharest, pp 159–160 (cuadrifasciata standing for quadrifasciata)
Mc Cabe SI, Ferro MWB, Farina WM, Hrncir M (2016) Dose-and time-dependent effects of oral octopamine treatments on the sucrose responsiveness in stingless bees (Melipona scutellaris). Apidologie. doi:10.1007/s13592-016-0442-x:1-7
Michener CD (2000) The bees of the world. The Johns Hopkins University Press, Baltimore Maryland
Moure JS (1975) Notas sobre as espécies de Melipona descritas por Lepeletier em 1836 (Hymenoptera, Apidae). Rev Bras Biol 35:615–623
Nieh JC (2004) Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 35:159–182
Nieh JC, Roubik DW (1995) A stingless bee (Melipona panamica) indicates food location without using a scent trail. Behav Ecol Sociobiol 37:36–70
Nogueira-Neto P (1970) A criação de abelhas indígenas sem ferrão, 2nd edn. Chácaras e Quintais, São Paulo
Nogueira-Neto P (1997) Vida e criação de abelhas indígenas sem ferrão. Editora Nogueirapis, São Paulo
Noll FB (2002) Behavioral phylogeny of corbiculate Apidae (Hymenoptera; Apinae), with special reference to social behavior. Cladistics 18:137–153
Peres-Neto PR, Olden JD (2001) Assessing the robustness of randomization tests: examples from behavioural studies. Anim Behav 61:79–86
Pick R, Blochtein B (2002) Atividades de vôo de Plebeia saiqui (Holmberg) (Hymenoptera, Apidae, Meliponini) durante o período de postura da rainha e em diapausa. Rev Bras Zool 19:827–839
Pierrot LM, Schlindwein C (2003) Variation in daily flight activity and foraging patterns in colonies of uruçu—Melipona scutellaris Latreille (Apidae, Meliponini). Rev Bras Zool 20:565–571
R Development Core Team (2003) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0
Ribeiro MF, Imperatriz-Fonseca VL, Filho PSS (2003) A interrupção da construção de células de cria e postura em Plebeia remota (Holmberg) (Hymenoptera, Apidae, Meliponini). In: Melo GAR, Santos IA (eds) Apoidea neotropica. Editora UNESC, Circiúma, pp 177–188
Rinderer TE (1981) Volatiles from empty comb increase hoarding by honeybee. Anim Behav 29:1275–1276
Rinderer TE (1982) Regulated nectar harvesting by the honeybee. J Apic Res 21:74–87
Rinderer TE (1983) Regulation of honey bee hoarding efficiency. Apidologie 14:87–92
Rinderer TE, Baxter JR (1978) Effect of empty comb on hoarding behavior and honey production of the honey bee. J Econ Entomol 71:757–759
Rinderer TE, Baxter JR (1979) Honey bee hoarding behaviour: effects of previous stimulation by empty comb. Anim Behav 27:426–428
Roubik DW (1982) Seasonality in colony food storage, brood production and adult survivorship: studies of Melipona in tropical forest (Hymenoptera: apidae). J Kansas Entomol Soc 55:789–800
Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, New York
Roubik DW, Peralta FJA (1983) Thermodynamics in nests of two Melipona species in Brazil. Acta Amazônica 13:453–466
Sakagami SF (1982) Stingless bees. In: Hermann HR (ed) Social insects, vol 3. Academic Press, New York, pp 361–423
Schmidt VM, Schorkopf DLP, Hrncir M, Zucchi R, Barth FG (2006) Collective foraging in a stingless bee: dependence on food profitability and sequence of discovery. Anim Behav 72:1309–1317
Schmidt VM, Hmcir M, Schorkopf DLP, Mateus S, Zucchi R, Barth FG (2008) Food profitability affects intranidal recruitment behaviour in the stingless bee Nannotrigona testaceicornis. Apidologie 39:260–272
Schorkopf DLP, Zucchi R, Barth FG (2004) Memory for feeding time. In: Proceedings of the 8th International Conference on Tropical Bees and VI Encontro sobre Abelhas. Ribeirão Preto, São Paulo. Brazil, p 643
Schorkopf DLP, Jarau S, Francke W, Twele R, Zucchi R, Hmcir M, Schmidt VM, Ayasse M, Barth FG (2007) Spitting out information: trigona bees deposit saliva to signal resource locations. Proc R Soc B 274:895–898
Schwarz HF (1948) Stingless bees (Meliponidae) of the western hemisphere. Bull Am Mus Nat Hist 90:1–546
Seeley TD (1985) Honeybee ecology: a study of adaptation in social life. Princeton University Press, US
Seeley TD (1989) Social foraging in honey bees: how nectar foragers assess their colony’s nutritional status. Behav Ecol Sociobiol 24:181–199
Seeley TD (1995) The wisdom of the hive: The social physiology of honey bee colonies. Harvard University Press, Cambridge, Massachusetts
Sokal RR, Rohlf J (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman, New York
van Veen JW, Arce HG, Sommeijer MJ (2004) Production of queens and drones in Melipona beecheii (Meliponini) in relation to colony development and resource availability. Proc Neth Entomol Soc 15:35–39
von Frisch K (1965) Tanzsprache und Orientierung der Bienen. Springer, NewYork
von Jacobs-Jessen UF (1959) Zur Orientierung der Hummeln und einiger anderer Hymenopteren. Z vergl Physiol 41:597–641
Winston ML (1987) The biology of the honey bee. Harvard University Press, Cambridge, Massachusetts
Zanella F (2000) The bees of the Caatinga (Hymenoptera, Apoidea, Apiformes): a species list and comparative notes regarding their distribution. Apidologie 31:579–592
Zucchi R (1993) Ritualized dominance, evolution of queen-worker interactions and related aspects in stingless bees (Hymenoptera: Apidae). In: Inoue T, Yamane S (eds) Evolution of insect societies: comparative sociology of bees, wasps and ants. Hakuhinsha, Tokyo, pp 207–249
Acknowledgments
This study was supported by Grants of the Austrian “Bundesministerium für Wissenschaft und Kunst” and “Internationales Büro” (University of Vienna) to DLPS, the Brazilian Science Foundation CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) under Grant 55/2013—Pró-Integração-AUXPE 3168/2013 to MH, the Brazilian Science Foundation CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) to CMS, and by Grant P14328 of the Austrian Science Foundation (FWF) to FGB. We are grateful to Prof. Z.L.P. Simões and the Departamento de Genetica (FMRP, USP) for their generous hospitality and Dr. Weyder Santana for helping handling the hives in Ribeirão Preto. We thank Prof. L. Bego for providing logistic support and M.A. Batista, Dr. S. Jarau, Dr. Sidnei Mateus, Prof. Ronaldo Zucchi, the late Prof. J.M.F. Camargo, and Prof. P.N. Neto for helpful discussions and encouragement after the first set of unexpected foraging results following honey store removal in both Melipona seminigra and M. scutellaris. We are particularly grateful to Dr. Hans Nemeschkal and Prof. Fred Bookstein for their very valuable help with permutation statistics. We greatly appreciate Prof. Tom D. Seeley’s suggestions that improved an earlier version of the manuscript focusing on aspects of recruitment behaviour. We also thank the anonymous reviewers for suggestions, which further improved our paper. Finally, we gratefully thank Rodrigo O.C. Carvalho and Dr. Airton T. Carvalho and their family for allowing us to conduct the multiple colony foraging experiments at Camaragibe, as well as for their assistance when preparing for the experiments.
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Schorkopf, D.L.P., de Sá Filho, G.F., Maia-Silva, C. et al. Nectar profitability, not empty honey stores, stimulate recruitment and foraging in Melipona scutellaris (Apidae, Meliponini). J Comp Physiol A 202, 709–722 (2016). https://doi.org/10.1007/s00359-016-1102-3
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DOI: https://doi.org/10.1007/s00359-016-1102-3