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Colony Function and Communication

  • José Javier G. Quezada-Euán
Chapter

Abstract

Workers of M. beecheii performing different activities in the brood area.

Keywords

Age polyethism Juvenile hormone Ecdysteroids Task allocation Task partition Life span Specialization Caste Subcaste Food transference Waste management POP Trophic egg Cleptobiosis Soldier Suicidal bite Aggressive response Resin Lactobacilli Immune system Hygienic behavior Semiochemical Scent mark Trail pheromone Cuticular hydrocarbon Nestmate recognition Food communication 

References

  1. Aguilar I, Briceño D (2002) Sounds in Melipona costaricensis (Apidae: Meliponini): effect of the sugar concentration and nectar source distance. Apidologie 33:375–388CrossRefGoogle Scholar
  2. Aguilar I, Sommeijer M (2001) The deposition of anal excretions by Melipona favosa foragers (Apidae: Meliponinae): behavioural observations concerning the location of food sources. Apidologie 32:37–48CrossRefGoogle Scholar
  3. Aparecido-Pereira R, Morais MM, Gioli LD, Santos NF, Rossi MA, Bego LR (2006) Comparative morphology of reproductive and trophic eggs in Melipona bees (Apidae, Meliponini). Braz J Morphol Sci 23:349–354Google Scholar
  4. Avila B, Moo-Valle H, Valladares P, Camposeco F, Quezada-Euán JJG (2005) Descripción del proceso de aprovisionamiento y oviposición en colonias de Melipona beecheii (Apidae: Meliponini). Reporte de investigación, opción apicultura. FMVZ-Universidad Autónoma de Yucatán, Maestría en Producción Animal TropicalGoogle Scholar
  5. Barth FG, Hrncir M, Jarau S (2008) Signals and cues in the recruitment behavior of stingless bees (Meliponini). J Comp Physiol A 194:313–327CrossRefGoogle Scholar
  6. Bian Z, Fales HM, Blum MS, Jones TH, Rinderer TE, Howard DF (1984) Chemistry of cephalic secretion of fire bee Trigona (Oxytrigona) tataira. J Chem Ecol 10:451–461PubMedCrossRefPubMedCentralGoogle Scholar
  7. Biesmeijer JC (1997) The organisation of foraging in stingless bees of the genus Melipona; an individual approach. Ph.D. thesis, Utrecht University, Utrecht, 263 ppGoogle Scholar
  8. Biesmeijer JC, Toth E (1998) Individual foraging, activity level and longevity in the stingless bee Melipona beecheii in Costa Rica (Hymenoptera, Apidae, Meliponinae). Insect Soc 45:427–443CrossRefGoogle Scholar
  9. Bigio G, Schürch R, Ratnieks FLW (2013) Hygienic behaviour in honey bees (Hymenoptera: Apidae): effects of brood, food, and time of the year. J Econ Entomol 106:2280–2285PubMedCrossRefPubMedCentralGoogle Scholar
  10. Billen J, Morgan ED (1998) Pheromone communication in social insects: sources and secretions. In: Vander Meer RK, Breed MD, Espelie KE, Winston ML (eds) Pheromone communication in social insects: ants, wasps, bees and termites. Westview Press, Boulder, pp 3–33Google Scholar
  11. Blum MS, Crewe RM, Kerr WE, Keith LH, Garrison AW, Walker MM (1970) Citral in stingless bees: isolation and functions in trail laying and robbing. J Insect Physiol 16:1637–1648PubMedCrossRefPubMedCentralGoogle Scholar
  12. Borges AA, Ferreira-Caliman MJ, Nascimento FS, Campos LAO, Tavares MG (2012) Characterization of cuticular hydrocarbons of diploid and haploid males, workers and queens of the stingless bee Melipona quadrifasciata. Insect Soc 59:479–486CrossRefGoogle Scholar
  13. Boogert NJ, Hofstede FE, Aguilar Monge I (2006) The use of food source scent marks by the stingless bee Trigona corvina (Hymenoptera: Apidae): the importance of the depositor’s identity. Apidologie 37:366–375CrossRefGoogle Scholar
  14. Breed MD, Butler L, Stiller TM (1985) Kin discrimination by worker honey bees in genetically mixed groups. Proc Natl Acad Sci USA 82:3058–3061PubMedCrossRefPubMedCentralGoogle Scholar
  15. Breed MD, Stocker EM, Baumgartner LK, Vargas E (2002) Time-place learning and the ecology of recruitment in a stingless bee, Tr. amalthea (Hymenoptera, Apidae). Apidologie 33:251–258CrossRefGoogle Scholar
  16. Breed MD, Cook C, Krasnec MO (2012) Cleptobiosis in social insects. Psyche. Article ID 484765Google Scholar
  17. Buchwald R, Breed MD (2005) Nestmate recognition cues in the stingless bee Trigona fulviventris. Anim Behav 70:1331–1337CrossRefGoogle Scholar
  18. Camargo JMF, Garcia MVB, Junior ERQ, Castrillon A (1992) Notas previas sobre a bionomia de Ptilotrigona lurida (Hymenoptera, Apidae, Meliponinae): associação de leveduras em pólen estocado. Boletim do Museu Paraense Emílio Goeldi 8:391–395Google Scholar
  19. Camargo JMF, Pedro SRM (2007) Meliponini Lepeletier, 1836. In: Moure JS (ed) Catalogue of the bees (Hymenoptera, Apoidea) in the Neotropical region. Sociedade Brasileira de Entomologia, Curitiba, pp 272–578Google Scholar
  20. Cardoso-Júnior CAM, Pereira Silva R, Araújo Borges N, de Carvalho WJ, Walter SL, Paulino Simões ZL, Bitondi MMG, Ueira Vieira C, Bonetti AM, Hartfelder K (2017a) Methyl farnesoate epoxidase (mfe) gene expression and juvenile hormone titers in the life cycle of a highly eusocial stingless bee, Melipona scutellaris. J Insect Physiol 101:185–194PubMedCrossRefPubMedCentralGoogle Scholar
  21. Cardoso-Júnior CAM, Fujimura PT, Santos-Júnior CD, Borges NA, Ueira-Vieira C, Hartfelder K, Goulart LR, Bonetti AM (2017b) Epigenetic modifications and their relation to caste and sex determination and adult division of labor in the stingless bee Melipona scutellaris. Genet Mol Biol 40(1):61–68PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chittka L, Thomson JD (2001) Cognitive ecology of pollination, animal behavior and floral evolution. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  23. Choo YM, Lee KS, Yoon HJ, Kim BY, Sohn MR et al (2010) Dual strategy of bee venom serine protease: prophenoloxidase-activating factor in arthropods and fibrin(ogen)olytic enzyme in mammals. PLoS One 5:e10393PubMedPubMedCentralCrossRefGoogle Scholar
  24. Couvillon MJ, Ratnieks FLW (2008) Odour transfer in stingless bee marmelada (Frieseomelitta varia) demonstrates that entrance guards use an ‘undesirable-absent’ recognition system. Behav Ecol Sociobiol 62:1099–1105CrossRefGoogle Scholar
  25. Crespi BJ (1992) Cannibalism and trophic eggs in subsocial and eusocial insects. In: Elgar MA, Crespi BJ (eds) Cannibalism, ecology and evolution among diverse taxa. Oxford University Press, Oxford, pp 176–213Google Scholar
  26. Cruz-Landim C (2000) Ovarian development in Meliponine bees (Hymenoptera: Apidae): the effect of queen presence and food on worker ovary development and egg production. Genet Mol Biol 23:83–88CrossRefGoogle Scholar
  27. Cruz-Landim C, Ferreira-Caliman MJ, Gracioli-Vitti LF, Zucchi R (2012) Correlation between mandibular gland secretion and cuticular hydrocarbons in the stingless bee Melipona quadrifasciata. Genet Mol Res 11:966–977PubMedCrossRefPubMedCentralGoogle Scholar
  28. Cruz-Lopez L, Malo EA, Morgan ED, Rincon M, Guzman M, Rojas JC (2005) Mandibular gland secretion of Melipona beecheii: chemistry and behavior. J Chem Ecol 31:1621–1632PubMedCrossRefPubMedCentralGoogle Scholar
  29. Cruz-Lopez L, Aguilar S, Malo EA, Rincon M, Guzman M, Rojas JC (2007) Electroantennogram and behavioral responses of workers of the stingless bee Oxytrigona mediorufa to mandibular gland volatiles. Entomol Exp Appl 123:43–47CrossRefGoogle Scholar
  30. Dade HA (1985) Anatomy and dissection of the honeybee. International Bee Research Association, LondonGoogle Scholar
  31. Daneels EL, Van Vaerenberg M, Debyser G, Devreese B, Graaf DC d (2015) Honeybee venom proteome profile of queens and winter bees as determined by a mass spectrometric approach. Toxins 7:4468–4483CrossRefGoogle Scholar
  32. Díaz S, de Souza Urbano S, Caesar L, Blochtein B, Sattler A, Zuge V, Haag KL (2017) Report on the microbiota of Melipona quadrifasciata affected by a recurrent disease. J Invertebr Pathol 143:35–39PubMedCrossRefGoogle Scholar
  33. dos Santos CG, Blochtein B, Megiolaro FL, Imperatriz-Fonseca VL (2010) Age Polyethism in Plebeia emerina (Friese) (Hymenoptera: Apidae) colonies related to propolis handling. Neotrop Entomol 39:691–696PubMedCrossRefPubMedCentralGoogle Scholar
  34. dos Santos CF, Ferreira-Caliman MJ, Nascimento FS (2015) An alien in the group: eusocial male bees sharing nonspecific reproductive aggregations. J Insect Sci 15:157PubMedPubMedCentralCrossRefGoogle Scholar
  35. Drumond PM, Zucchi R, Oldroyd BP (2000) Description of the cell provisioning and oviposition process of seven species of Plebeia Schwarz (Apidae, Meliponini), with notes on their phylogeny and taxonomy. Insect Soc 47:99–112CrossRefGoogle Scholar
  36. Eardley CD (2004) Taxonomic revision of the African stingless bees (Apoidea: Apidae: Apinae: Meliponini). Afr Plant Protect 10:63–96Google Scholar
  37. Engels W (1987) Pheromones and reproduction in Brazilian stingless bees. Memorias Instituto Oswaldo Cruz, Rio de Janeiro 82(Suppl III):35–45CrossRefGoogle Scholar
  38. Engels E, Engels W, Schroder W, Francke W (1987) Intranidal worker reactions to volatile compounds identified from cephalic secretions in the stingless bee, Scaptotrigona postica (Hymenoptera, Meliponinae). J Chem Ecol 13:371–386PubMedCrossRefPubMedCentralGoogle Scholar
  39. Engels W, Engels E, Lübke G, Schröder W, Francke W (1990) Volatile cephalic secretions of drones, queens and workers in relation to reproduction in the stingless bee, Scaptotrigona postica. Entomologia Generalis 15:91–101CrossRefGoogle Scholar
  40. Evans JD, Aronstein K, Chen YP, Hetru C, Imler JL, Jiang H, Kanost M et al (2006) Immune pathways and defence mechanisms in honeybees Apis mellifera. Insect Mol Biol 15:645–656PubMedPubMedCentralCrossRefGoogle Scholar
  41. Fierro MM, Cruz-López L, Sánchez D, Villanueva-Gutiérrez R, Vandame R (2011) Queen volatiles as a modulator of Tetragonisca angustula drone behavior. J Chem Ecol 37:1255–1262PubMedCrossRefPubMedCentralGoogle Scholar
  42. Flach A, Marsaioli AJ, Singer RB, Amaral M d CE, Menezes C, Kerr WE, Batista-Pereira LG, Correa AG (2006) Pollination by sexual mimicry in Mormolyca ringens: a floral chemistry that remarkably matches the pheromones of virgin queens of Scaptotrigona sp. J Chem Ecol 32:59–70PubMedCrossRefPubMedCentralGoogle Scholar
  43. Flaig IC, Aguilar I, Schmitt T, Jarau S (2016) An unusual recruitment strategy in a mass-recruiting stingless bee, Partamona orizabaensis. J Comp Physiol A 202:679–690CrossRefGoogle Scholar
  44. Francke W, Schroder W, Engels E, Engels W (1983) Variation in cephalic volatile substances in relation to worker age and behavior in the stingless bee, Scaptotrigona postica. Z Naturforsch 38c:1066–1068CrossRefGoogle Scholar
  45. Free JB (1987) Pheromones of social bees. Cornell University Press, IthacaGoogle Scholar
  46. Gibbs A (1995) Physical properties of insect curticular hydrocarbons: model mixtures and lipid interactions. Comp Biochem Physiol 112B:667–672CrossRefGoogle Scholar
  47. Gibbs A, Pomonis JG (1995) Physical properties of insect cuticular hydrocarbons: the effects of chain length, methyl-branching and unsaturation. Comp Biochem Physiol 112B:243–249CrossRefGoogle Scholar
  48. Gloag R, Heard T, Beekman M, Oldroyd B (2008) Nest defence in a stingless bee: what causes fighting swarms in Trigona carbonaria (Hymenoptera, Meliponini)? Insect Soc 55:387–391CrossRefGoogle Scholar
  49. Gordon DM (2016) From division of labor to the collective behavior of social insects. Behav Ecol Sociobiol 70:1101–1108PubMedCrossRefGoogle Scholar
  50. Goulson D, Chapman JW, Hughes WOH (2001) Discrimination of unrewarding flowers by bees; direct detection of rewards and use of repellent scent marks. J Insect Behav 14:669–678CrossRefGoogle Scholar
  51. Greco MK, Hoffmann D, Dollin A, Duncan M, Spooner-Hart R, Neumann P (2010) The alternative pharaoh approach: stingless bees mummify beetle parasites alive. Naturwissenschaften 97:319–323PubMedCrossRefGoogle Scholar
  52. Grüter C, Menezes C, Imperatriz-Fonseca VL, Ratnieks FLW (2012) A morphologically specialized soldier caste improves colony defence in a Neotropical eusocial bee. Proc Natl Acad Sci USA 109:1182–1186PubMedCrossRefPubMedCentralGoogle Scholar
  53. Grüter C, Keller L (2016) Inter-caste communication in social insects. Curr Opin Neurobiol 38:6–11PubMedCrossRefPubMedCentralGoogle Scholar
  54. Grüter C, von Zuben LG, Segers FHID, Cunningham JP (2016) Warfare in stingless bees. Insect Soc 63:223–236CrossRefGoogle Scholar
  55. Grüter C, Segers FHID, Menezes C, Vollet-Neto A, Falcón T, von Zuben L, Bitondi MMG, Nascimento FS, Almeida EAB (2017) Repeated evolution of soldier sub-castes suggests parasitism drives social complexity in stingless bees. Nat Commun 8:4PubMedPubMedCentralCrossRefGoogle Scholar
  56. Gutiérrez E, Ruiz D, Solís T, May-Itzá W d J, Moo-Valle H, Quezada Euán JJG (2016) Does larval food affect cuticular profiles and recognition in eusocial bees? A test on Scaptotrigona gynes (Hymenoptera: Meliponini). Behav Ecol Sociobiol 70:781–789CrossRefGoogle Scholar
  57. Hart AG, Ratnieks FLW (2001) Why do honey-bee (Apis mellifera) foragers transfer nectar to several receivers? Information improvement through multiple sampling in a biological system. Behav Ecol Sociobiol 49:244–250CrossRefGoogle Scholar
  58. Hart AG, Ratnieks FLW (2002) Task partitioned nectar transfer in stingless bees (Meliponini): work organisation in a phylogenetic context. Ecol Entomol 27:163–168CrossRefGoogle Scholar
  59. Hartfelder K, Bitondi MMG, Santana WC, Simões ZLP (2002) Ecdysteroid titers and reproduction in queens and workers of the honey bee and of a stingless bee: loss of ecdysteroid function at increasing levels of sociality? J Insect Physiol 32:211–216Google Scholar
  60. Hartfelder K, Makert GR, Judice CC, Pereira GAG, Santana WC, Dallacqua R, Bitondi MMG (2006) Physiological and genetic mechanisms underlying caste development, reproduction and division of labor in stingless bees. Apidologie 37:144–163CrossRefGoogle Scholar
  61. Hermann HR (1984) Defensive mechanisms: general considerations. In: Hermann HR (ed) Defensive mechanisms in social insects. Praeger, New York, pp 1–31Google Scholar
  62. Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, CambridgeCrossRefGoogle Scholar
  63. Hrncir M, Jarau S, Zucchi R, Barth FG (2000) Recruitment behavior in stingless bees, Melipona scutellaris and M. quadrifasciata. II. Possible mechanisms of communication. Apidologie 31:93–113CrossRefGoogle Scholar
  64. Hrncir M, Jarau S, Zucchi R, Barth FG (2003) A stingless bee (Melipona seminigra) uses optic flow to estimate flight distances. J Comp Physiol 189:761–768CrossRefGoogle Scholar
  65. 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 35:3–13CrossRefGoogle Scholar
  66. 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 190:549–560Google Scholar
  67. Hrncir M, Schmidt VM, Schorkopf DLP, Jarau S, Zucchi R, Barth FG (2006) Vibrating the food receivers: a direct way of signal transmission in stingless bees (Melipona seminigra). J Comp Physiol A 192:879–887CrossRefGoogle Scholar
  68. 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 223–250CrossRefGoogle Scholar
  69. Jarau S, Hrncir M, Ayasse M, Schulz C, Francke W, Zucchi R, Barth FG (2004) A stingless bee (Melipona seminigra) marks food sources with a pheromone from its claw retractor tendons. J Chem Ecol 30:793–804PubMedCrossRefPubMedCentralGoogle Scholar
  70. Jarau S, Schulz CM, Hrncir M, Francke W, Zucchi R, Barth FG, Ayasse M (2006) Hexyl decanoate, the first trail pheromone compound identified in a stingless bee, Trigona recursa. J Chem Ecol 32:1555–1564PubMedCrossRefPubMedCentralGoogle Scholar
  71. Johnson LK, Haynes LW, Carlson MA, Fortnum HA, Gorgas DL (1985) Alarm substances of the stingless bee, Trigona silvestriana. J Chem Ecol 11:409–416PubMedCrossRefPubMedCentralGoogle Scholar
  72. Jones SM, van Zweden JS, Grüter C, Menezes C, Alves DA, Nunes-Silva P, Czaczkes T, Imperatriz-Fonseca VL, Ratnieks FLW (2012) The role of wax and resin in the nestmate recognition system of a stingless bee, Tetragonisca angustula. Behav Ecol Sociobiol 66:1–12CrossRefGoogle Scholar
  73. Jungnickel H, Velthuis HHW, Imperatriz-Fonseca VL, Morgan ED (2001) Chemical properties allow stingless bees to place their eggs upright on liquid larval food. Physiol Entomol 26:300–305CrossRefGoogle Scholar
  74. Jungnickel H, da Costa AJS, Tentschert J, Flávia E, Patricio LRA, Imperatriz-Fonseca VL, Drijfhout F, Morgan ED (2004) Chemical basis for inter-colonial aggression in the stingless bee Scaptotrigona bipunctata (Hymenoptera: Apidae). J Insect Physiol 50:761–766PubMedCrossRefPubMedCentralGoogle Scholar
  75. Keeping MG, Crewe RM, Field BI (1982) Mandibular secretions of the old world stingless bee, Trigona gribodoi Magrettii: isolation, identification, and compositional changes with age. J Apic Res 21:65–73CrossRefGoogle Scholar
  76. Kerr WE, Lello E (1962) Sting glands in stingless bees—a vestigial character. J NY Entomol Soc 70:190–214Google Scholar
  77. Kerr WE, Rocha R (1988) Communicação em Melipona rufiventris e Melipona compressipes. Ciência e Cultura 40:1200–1202Google Scholar
  78. Kirchner WH, Lindauer M (1994) The causes of the tremble dance. Behav Ecol Sociobiol 35:303–308CrossRefGoogle Scholar
  79. Koedam D, Velthausz PH, van de Krift T, Dohmen MR, Sommeijer MJ (1996) Morphology of reproductive and trophic eggs and their controlled release by workers in Trigona (Tetragonisca) angustula Illiger (Apidae, Meliponinae). Physiol Entomol 21:289–296CrossRefGoogle Scholar
  80. Koethe S, Bossems J, Dyer AG, Lunau K (2016) Colour is more than hue: preferences for compiled colour traits in the stingless bees Melipona mondury and M. quadrifasciata. J Comp Physiol A 202:615–627CrossRefGoogle Scholar
  81. Kolmes SA (1985) An information-theory analysis of task specialization among worker honey bees performing hive duties. Anim Behav 33:181–187CrossRefGoogle Scholar
  82. Kwong WK, Medina LA, Koch H, Sing KW, Yu Soh EJ, Ascher JS, Jaffé R, Moran NA (2017) Dynamic microbiome evolution in social bees. Sci Adv 3:e1600513PubMedPubMedCentralCrossRefGoogle Scholar
  83. Lapidge K, Oldroyd B, Spivak M (2002) Seven suggestive quantitative trait loci influence hygienic behavior of honeybees. Naturwissenschaften 89:565–568PubMedPubMedCentralGoogle Scholar
  84. Lenoir A, D’Ettorre P, Errard C (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599PubMedCrossRefPubMedCentralGoogle Scholar
  85. Leonhardt SD, Blüthgen N (2009) A sticky affair: resin collection by Bornean stingless bees. Biotropica 41:730–736CrossRefGoogle Scholar
  86. Leonhardt SD, Kaltenpoth M (2014) Microbial communities of three sympatric Australian stingless bee species. PLoS One 9:e105718PubMedPubMedCentralCrossRefGoogle Scholar
  87. Leonhardt SD, Jung LM, Schmitt T, Blüthgen N (2010a) Terpenoids tame aggressors: role of chemicals in stingless bee communal nesting. Behav Ecol Sociobiol 64:1415–1423CrossRefGoogle Scholar
  88. Leonhardt SD, Zeilhofer S, Schmitt T (2010b) Stingless bees use terpenes as olfactory cues to find resin sources. Chem Senses 35:603–611PubMedCrossRefPubMedCentralGoogle Scholar
  89. Leonhardt SD, Wallace HM, Blüthgen N, Wenzel F (2015) Potential role of environmentally derived cuticular compounds in stingless bees. Chemoecology 25:159–167CrossRefGoogle Scholar
  90. Lichtenberg EM, Hrncir M, Turatti IC, Nieh JC (2011) Olfactory eavesdropping between two competing stingless bee species. Behav Ecol Sociobiol 65:763–774PubMedCrossRefPubMedCentralGoogle Scholar
  91. Lindauer M, Kerr WE (1960) Communication between the workers of stingless bees. Bee World 41:29–41–65–71CrossRefGoogle Scholar
  92. López-Uribe MM, Sconiers WB, Frank SD, Dunn RR, Tarpy DR (2016) Reduced cellular immune response in social insect lineages. Biol Lett 12:20150984PubMedPubMedCentralCrossRefGoogle Scholar
  93. Machado JO (1971) Simbiose entre as abelhas sociais brasileiras (Meliponinae, Apidae) e uma espécie de bactéria. Ciência e Cultura 23:625–633Google Scholar
  94. Martin SJ, Jenner EA, Drijfhout FP (2007) Chemical deterrent enables a social parasitic ant to invade multiple hosts. Proc R Soc B 274:2717–2721PubMedCrossRefPubMedCentralGoogle Scholar
  95. Martin SJ, Carruthers JM, Williams PH, Drijfhout FP (2010) Host specific social parasites (Psithyrus) indicate chemical recognition system in bumblebees. J Chem Ecol 36:855–863PubMedCrossRefPubMedCentralGoogle Scholar
  96. Martin SJ, Shemilt S, da S Lima CB, de Carvalho CAL (2017) Are isomeric alkenes used in species recognition among neo-tropical stingless bees (Melipona spp). J Chem Ecol 43:1066–1072Google Scholar
  97. McFrederick SQ, Cannone JJ, Gutell RR, Kellner K, Plowes RM, Mueller UG (2013) Specificity between lactobacilli and hymenopteran hosts is the exception rather than the rule. Appl Environ Microbiol 79:1803–1812PubMedPubMedCentralCrossRefGoogle Scholar
  98. McFrederick SQ, Wcislo WT, Taylor DR, Ishak HD, Dowd SE et al (2012) Environment or kin: whence do bees obtain acidophilic bacteria? Mol Ecol Notes 21:1754–1768CrossRefGoogle Scholar
  99. Medina-Medina LA, Hart AG, Ratnieks FLW (2009) Hygienic behavior in the stingless bees Melipona beecheii and Scaptotrigona pectoralis (Hymenoptera: Meliponini). Genet Mol Res 8:571–576CrossRefGoogle Scholar
  100. Medina-Medina LA, Hart AG, Ratnieks FLW (2014) Waste management in the stingless bee Melipona beecheii Bennett (Hymenoptera: Apidae). Sociobiology 61:428–434CrossRefGoogle Scholar
  101. Medina RG, Fairbairn DJ, Bustillos A, Moo-Valle H, Medina S, Quezada-Euán JJG (2016) Variable patterns of intraspecific sexual size dimorphism and allometry in three species of eusocial corbiculate bees. Insect Soc 63:493–500CrossRefGoogle Scholar
  102. Menezes C, Vollet-Neto A, León Contrera FA, Venturieri GC, Imperatriz-Fonseca VL (2013) The role of useful microorganisms to stingless bees and stingless beekeeping. In: Vit P, Pedro SRM, Roubik DW (eds) Pot honey: a legacy of stingless bees. Springer, New York, pp 153–172CrossRefGoogle Scholar
  103. Menezes C, Vollet-Neto A, Marsaioli AJ, Zampieri D, Fontoura IC, Luchessi AD, Imperatriz-Fonseca VL (2015) A Brazilian social bee must cultivate fungus to survive. Curr Biol 25:2851–2855PubMedCrossRefPubMedCentralGoogle Scholar
  104. Michener CD (1974) The social behavior of the bees: a comparative study. Belknap Press, Harvard University, CambridgeGoogle Scholar
  105. Morais PB, Calaça PSST, Rosa CA (2013) Microorganisms associated with stingless bees. In: Vit P, Pedro SRM, Roubik DW (eds) Pot honey: a legacy of stingless bees. Springer, New York, pp 173–186CrossRefGoogle Scholar
  106. Nascimento DL, Nascimento FS (2012) Acceptance threshold hypothesis is supported by chemical similarity of cuticular hydrocarbons in a stingless bee, Melipona asilvai. J Chem Ecol 38:1432–1440PubMedCrossRefPubMedCentralGoogle Scholar
  107. Nash DR, Boomsma JJ (2008) Communication between hosts and social parasites. In: D’Ettorre P, Hughes DP (eds) Sociobiology of communication: an interdisciplinary perspective. Oxford University Press, Oxford, pp 55–80CrossRefGoogle Scholar
  108. Nieh JC (1998) The role of a scent beacon in the communication of food location by the stingless bee, Melipona panamica. Behav Ecol Sociobiol 43:47–58CrossRefGoogle Scholar
  109. Nieh JC (2004) Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 35:159–182CrossRefGoogle Scholar
  110. Nieh JC, Roubik DW (1995) A stingless bee (Melipona panamica) indicates food location without using a scent trail. Behav Ecol Sociobiol 37:63–70CrossRefGoogle Scholar
  111. Nieh JC, Roubik DW (1998) Potential mechanisms for the communication of height and distance by a stingless bee, Melipona panamica. Behav Ecol Sociobiol 43:387–399CrossRefGoogle Scholar
  112. Nieh JC, Tautz J, Spaethe J, Bartareau T (1999) The communication of food location by a primitive stingless bee, Trigona carbonaria. Zoology 102:238–246Google Scholar
  113. Nieh JC, Contrera FAL, Rangel J, Imperatriz-Fonseca VL (2003) Effect of food location and quality on recruitment sounds and success in two stingless bees, Melipona mandacaia and Melipona bicolor. Behav Ecol Sociobiol 55:87–94CrossRefGoogle Scholar
  114. Nieh JC, Barreto LS, Contrera FAL, Imperatriz-Fonseca VL (2004) Olfactory eavesdropping by a competitively foraging stingless bee, Trigona spinipes. Proc R Soc Lond B 271:1633–1640CrossRefGoogle Scholar
  115. Nunes TM, Nascimento FS, Turatti IC, Lopes NP, Zucchi R (2008) Nestmate recognition in a stingless bee: does the similarity of chemical cues determine guard acceptance? Anim Behav 75:1165–1171CrossRefGoogle Scholar
  116. Nunes TM, Turatti IC, Lopes NP, Zucchi R (2009a) Chemical signals in the stingless bee, Frieseomelitta varia, indicate caste, gender, age, and reproductive status. J Chem Ecol 35:1172–1180PubMedCrossRefPubMedCentralGoogle Scholar
  117. Nunes TM, Turatti IC, Mateus S, Nascimento FS, Lopes NP, Zucchi R (2009b) Cuticular hydrocarbons in the stingless bee Schwarziana quadripunctata (Hymenoptera, Apidae, Meliponini): differences between colonies, castes and age. Genet Mol Res 8:589–595PubMedCrossRefPubMedCentralGoogle Scholar
  118. Nunes TM, Mateus S, Turatti IC, Morgan E, Zucchi R (2011) Nestmate recognition in the stingless bee Frieseomelitta varia (Hymenoptera, Apidae, Meliponini): sources of chemical signals. Anim Behav 81:463–467CrossRefGoogle Scholar
  119. Nunes TM, Mateus S, Favaris AP, Amaral MFZJ, von Zuben LG, Clososki GC, Bento JMS, Oldroyd BP, Silva R, Zucchi R, Silva DB, Lopes NP (2014a) Queen signals in a stingless bee: suppression of worker ovary activation and spatial distribution of active compounds. Sci Rep 4:7449PubMedPubMedCentralCrossRefGoogle Scholar
  120. Nunes TM, von Zuben LG, Costa L, Venturieri GC (2014b) Defensive repertoire of the stingless bee Melipona flavolineata Friese (Hymenoptera: Apidae). Sociobiology 61:541–546CrossRefGoogle Scholar
  121. Nunes-Silva PN, Imperatriz-Fonseca VL, Gonçalves LS (2009) Hygienic behavior of the stingless bee Plebeia remota (Holmberg, 1903) (Apidae, Meliponini). Genet Mol Res 8:649–654PubMedCrossRefPubMedCentralGoogle Scholar
  122. Packer L (2003) Comparative morphology of the skeletal parts of the sting apparatus of bees (Hymenoptera: Apoidea). Zool J Linnean Soc 138:1–38CrossRefGoogle Scholar
  123. Page RE Jr (2013) The spirit of the hive: the mechanisms of social evolution. Harvard University Press, CambridgeCrossRefGoogle Scholar
  124. Page RE Jr, Metcalf RA, Erickson EH Jr, Lampman RL (1991) Extractable hydrocarbons and kin recognition in the honey bee (Apis mellifera L.). J Chem Ecol 17:745–756PubMedCrossRefPubMedCentralGoogle Scholar
  125. Patricio EFLRA, Cruz-López L, Morgan ED (2002) Electroantennography in the study of two stingless bee species (Hymenoptera: Meliponini). Braz J Biol 64:827–831CrossRefGoogle Scholar
  126. Perry JC, Roitberg BD (2006) Trophic egg laying: hypotheses and tests. Oikos 112:706–714CrossRefGoogle Scholar
  127. Pianaro A, Flach A, Patricio EFLRA, Nogueira-Neto P, Marsaioli AJ (2007) Chemical changes associated with the invasion of a Melipona scutellaris colony by Melipona rufiventris workers. J Chem Ecol 33:971–984PubMedCrossRefPubMedCentralGoogle Scholar
  128. Pianaro A, Menezes C, Kerr WE, Singer RB, Patricio EFLRA, Marsaioli AJ (2009) Stingless bees: chemical differences and potential functions in Nannotrigona testaceicornis and Plebeia droryana males and workers. J Chem Ecol 35:1117–1128PubMedCrossRefPubMedCentralGoogle Scholar
  129. Poiani SB, Morgan ED, Drijfhout FP, Cruz-Landim Cd (2014) Separation of Scaptotrigona postica workers into defined task groups by the chemical profile on their epicuticle wax layer. J Chem Ecol 40:331–340PubMedCrossRefPubMedCentralGoogle Scholar
  130. Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Timber Press, PortlandGoogle Scholar
  131. Quezada-Euán JJG, González-Acereto JA (2002) Notes on the nest habits and host range of cleptobiotic Lestrimelitta niitkib (Ayala 1999) (Hymenoptera: Meliponini) from the Yucatán peninsula, México. Acta Zool Mex 86:245–249Google Scholar
  132. Quezada-Euán JJG, López-Velasco A, Pérez-Balam J, Moo-Valle H, Velazquez-Madrazo A, Paxton RJ (2011) Body size differs in workers produced across time and is associated with variation in the quantity and composition of larval food in Nannotrigona perilampoides (Hymenoptera, Meliponini). Insect Soc 58:31–38CrossRefGoogle Scholar
  133. Quezada-Euán JJG, Ramírez J, Eltz T, Pokorny T, Medina R, Monsreal R (2013) Does sensory deception matter in eusocial obligate food robber systems? A study of Lestrimelitta and stingless bee hosts. Anim Behav 85:817–823CrossRefGoogle Scholar
  134. Quezada-Euán JJG, May-Itzá WdJ, Montejo E, Moo-Valle H (2015) Isometric worker size variation in relation to individual foraging preference and seasonal colony growth in stingless bees. Insect Soc 62:73–80CrossRefGoogle Scholar
  135. Raguso RA (2001) Floral scent, olfaction, and scent-driven foraging behavior. In: Chittka L, Thomson JD (eds) Cognitive ecology of pollination: animal behavior and floral evolution. Cambridge University Press, Cambridge, pp 83–105CrossRefGoogle Scholar
  136. Rasmussen C, Cameron SA (2010) Global stingless bee phylogeny supports ancient divergence, vicariance, and long distance dispersal. Biol J Linn Soc 99:206–232CrossRefGoogle Scholar
  137. Ratnieks FLW, Anderson C (1999) Task partitioning in insect societies. II. Use of queueing delay information in recruitment. Am Nat 154:536–548PubMedCrossRefPubMedCentralGoogle Scholar
  138. Riveros AJ, Groenenberg W (2010) Sensory allometry, foraging task specialization and resource exploitation in honeybees. Behav Ecol Sociobiol 64:955–966CrossRefGoogle Scholar
  139. Robinson GE, Huang ZY (1998) Colony integration in honey bees: genetic, endocrine and social control of division of labor. Apidologie 29:159–170CrossRefGoogle Scholar
  140. Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  141. Roubik DW, Smith BH, Carlson RG (1987) Formic acid in caustic cephalic secretions of stingless bee Oxytrigona (Hymenoptera: Apidae). J Chem Ecol 13:1079–1086PubMedCrossRefPubMedCentralGoogle Scholar
  142. Rothenbuhler WC (1964) Behavior genetics of nest cleaning in honey bees. IV. Responses of F1 and backcross generations to disease-killed brood. Am Zool 12:578–583Google Scholar
  143. Sakagami SF (1982) Stingless bees. In: Hermann HR (ed) Social insects, vol III. Academic Press, London, pp 361–423CrossRefGoogle Scholar
  144. Sakagami SF, Zucchi R (1966) Estudo comparativo do comportamento de varias especies de abelhas sem ferrão, com especial referencia oa processo de aprovisionamento e postura das celulas (Comparative study of various stingless bees behaviour with special provitioning reference process and cell posture). Ciencia e Cultura 18:283–296Google Scholar
  145. Sakagami SF, Roubik DW, Zucchi R (1993) Ethology of the robber stingless bee, Lestrimelitta limao (Hymenoptera: Apidae). Sociobiology 21:237–277Google Scholar
  146. Shackleton K, Toufailia A, Balfour NJ, Nasciento FS, Alves DA, Ratnieks FLW (2015) Appetite for self-destruction: suicidal biting as a nest defense strategy in Trigona stingless bees. Behav Ecol Sociobiol 69:273–281PubMedCrossRefPubMedCentralGoogle Scholar
  147. Schmidt VM, Hrncir M, Schorkopf DLP, Mateus S, Zucchi R, Barth FG (2008) Food profitability affects intranidal recruitment behaviour in the stingless bee Nannotrigona testaceicornis. Apidologie 39:260–272CrossRefGoogle Scholar
  148. Schorkopf DLP, Jarau S, Francke W, Twele R, Zucchi R, Hrncir M, Schmidt VM, Ayasse M, Barth FG (2007) Spitting out information: Trigona bees deposit saliva to signal resource locations. Proc R Soc B 274:895–898PubMedCrossRefPubMedCentralGoogle Scholar
  149. Schorkopf DLP, Hrncir M, Mateus S, Zucchi R, Schmidt VM, Barth FG (2009) Mandibular gland secretions of Meliponine worker bees: further evidence for their role in interspecific and intraspecific defence and aggression and against their role in food source signalling. J Exp Biol 212:1153–1162PubMedCrossRefPubMedCentralGoogle Scholar
  150. Schorkopf DLP (2016) Male Meliponine bees (Scaptotrigona aff. depilis) produce alarm pheromones to which workers respond with fight and males with flight. J Comp Physiol A 202:667–678CrossRefGoogle Scholar
  151. Seeley TD (1985) Honeybee ecology, a study of adaptation in social life. Princeton University Press, PrincetonCrossRefGoogle Scholar
  152. Seeley TD (1995) The wisdom of the hive, the social physiology of honeybee colonies. Harvard University Press, CambridgeGoogle Scholar
  153. Seeley TD (1998) Thoughts on information and integration in honey bee colonies. Apidologie 29:67–80CrossRefGoogle Scholar
  154. Septanil MPB, Mateus S, Turatti IT, Nunes TM (2012) Mixed colonies of two species of congeneric stingless bees (Hymenoptera: Apinae, Meliponini) display environmentally-acquired and endogenously-produced recognition signals. Physiol Entomol 37:72–80CrossRefGoogle Scholar
  155. Simone-Finstrom M, Spivak M (2010) Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41:295–311CrossRefGoogle Scholar
  156. Smith BH, Roubik DW (1983) Mandibular glands of stingless bees (Hymenoptera: Apidae): chemical analysis of their contents and biological function in two species of Melipona. J Chem Ecol 9:1465–1472PubMedCrossRefPubMedCentralGoogle Scholar
  157. Sommeijer MJ (1984) Distribution of labour among workers of Melipona favosa F: age polyethism and worker oviposition. Insect Soc 31:171–184CrossRefGoogle Scholar
  158. Sommeijer MJ (1987) Age-polyethism in stingless bees and evidence of flexible individual ontogenetic sequences. In: Eder J, Rembold H (eds) Chemistry and biology of social insects. Peperny, München, pp 129–130Google Scholar
  159. Sommerlandt FMJ, Huber W, Spaethe J (2014) Social information in the stingless bee, Trigona corvina Cockerell (Hymenoptera: Apidae): the use of visual and olfactory cues at the food site. Sociobiology 61:401–406CrossRefGoogle Scholar
  160. Spivak M, Downey DL (1998) Field assays for hygienic behavior in honey bees (Hymenoptera: Apidae). J Econ Entomol 91:64–70CrossRefGoogle Scholar
  161. Tofilski A (2002) Influence of age polyethism on longevity of workers in social insects. Behav Ecol Sociobiol 51:234–237CrossRefGoogle Scholar
  162. Toufailia HA, Alves DA, Bento JMS, Marchini LC, Ratnieks FLW (2016) Hygienic behaviour in Brazilian stingless bees. Biol Open 5:1712–1718PubMedPubMedCentralCrossRefGoogle Scholar
  163. Vander Meer RK, Morel L (1998) Nestmate recognition in ants. In: Vander Meer RK (ed) Pheromone communication in social insects: ants, wasps, bees and termites. Westview Press, Boulder, pp 79–103Google Scholar
  164. van Veen JW (2000) Cell provisioning and oviposition in Melipona beecheii (Apidae, Meliponinae), with a note on caste determination. Apidologie 31:411–419CrossRefGoogle Scholar
  165. van Veen JW, Sommeijer MJ, Meeuwsen F (1997) Behaviour of drones in Melipona (Apidae, Meliponinae). Insect Soc 44:435–447CrossRefGoogle Scholar
  166. van Zweden JS, D’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. In: Blomquist GJ, Bagnères AG (eds) Insect hydrocarbons: biology, biochemistry and chemical ecology. Cambridge University Press, Cambridge, pp 222–243CrossRefGoogle Scholar
  167. Vásquez A, Forsgren E, Fries I, Paxton RJ, Flaberg E, Szekely L, Olofsson TC (2012) Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS One 7:e33188PubMedPubMedCentralCrossRefGoogle Scholar
  168. Velthuis HHW (1997) The biology of stingless bees. Dept. of Ethology, Utrecht University, UtrechtGoogle Scholar
  169. Velthuis HHW, Cortopassi-Laurino M, Pereboom Z, Imperatriz-Fonzeca VL (2003) The conservative egg of the genus Melipona and its consequences for speciation. In: Melo GAR, Alves-dos-Santos I (eds) Apoidea Neotropica: Homenagem aos 90 Anos de Jesus Santiago Moure. Editora UNESC, Criciúma, pp 171–176Google Scholar
  170. Velthuis HHW, Koedam D, Imperatriz-Fonseca VL (2005) The males of Melipona and other stingless bees, and their mothers. Apidologie 36:169–185CrossRefGoogle Scholar
  171. von Zuben LG, Schorkopf DLP, Elias LG, Vaz ALL, Favaris AP, Clososki GC, Bento JMS, Nunes TM (2016) Interspecific chemical communication in raids of the robber bee Lestrimelitta limao. Insect Soc 63:339–347CrossRefGoogle Scholar
  172. Verdugo-Dardón M, Cruz-López L, Malo EA, Rojas JC, Guzmán-Díaz M (2011) Olfactory attraction of Scaptotrigona mexicana drones to their virgin queen volatiles. Apidologie 42:543–550CrossRefGoogle Scholar
  173. Villa JD, Weiss MR (1990) Observations on the use of visual and olfactory cues by Trigona spp foragers. Apidologie 21:541–545CrossRefGoogle Scholar
  174. Waddington KD (1989) Implications of variation in worker body size for the honey bee recruitment system. J Insect Behav 2:91–103CrossRefGoogle Scholar
  175. Wille A (1979) Phylogeny and relationships among the genera and subgenera of the stingless bees (Meliponinae) of the world. Rev Biol Trop 27:241–277Google Scholar
  176. Wille A (1983) Biology of the stingless bees. Annu Rev Entomol 28:41–64CrossRefGoogle Scholar
  177. Wilson EO (1971) The insect societies. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  178. Wilson EO (1990) Success and dominance in ecosystems: the case of the social insects. In: Kinne O (ed) Excellence in ecology. Book 2. Ecology Institute, Oldendorf/LuheGoogle Scholar
  179. Winston ML (1987) The biology of the honey bee. Harvard University Press, CambridgeGoogle Scholar
  180. Wyatt TD (2003) Pheromones and animal behaviour. Communication by smell and taste. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  181. Zucchi R (1993) Ritualized dominance, evolution of queen-worker interactions and related aspects in stingless bees. (Hym., Apidae). In: Sakagami SF, Inoue T, Yamane S (eds) Evolution of insect societies. Hakuhinsha, Tokyo, pp 207–249Google Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • José Javier G. Quezada-Euán
    • 1
  1. 1.Departamento de Apicultura Tropical, Campus de Ciencias Biológicas y AgropecuariasUniversidad Autónoma de YucatánMéridaMexico

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