Advertisement

Journal of Chemical Ecology

, Volume 43, Issue 4, pp 385–402 | Cite as

Chemical Ecology of Stingless Bees

  • Sara Diana Leonhardt
Article

Abstract

Stingless bees (Hymenoptera, Apidae: Meliponini) represent a highly diverse group of social bees confined to the world’s tropics and subtropics. They show a striking diversity of structural and behavioral adaptations and are important pollinators of tropical plants. Despite their diversity and functional importance, their ecology, and especially chemical ecology, has received relatively little attention, particularly compared to their relative the honeybee, Apis mellifera. Here, I review various aspects of the chemical ecology of stingless bees, from communication over resource allocation to defense. I list examples in which functions of specific compounds (or compound groups) have been demonstrated by behavioral experiments, and show that many aspects (e.g., queen-worker interactions, host-parasite interactions, neuronal processing etc.) remain little studied. This review further reveals that the vast majority of studies on the chemical ecology of stingless bees have been conducted in the New World, whereas studies on Old World stingless bees are still comparatively rare. Given the diversity of species, behaviors and, apparently, chemical compounds used, I suggest that stingless bees provide an ideal subject for studying how functional context and the need for species specificity may interact to shape pheromone diversification in social insects.

Keywords

Aggression Cuticular hydrocarbons Defensive strategies Nutritional chemistry Queen pheromones Plant-insect interactions 

Notes

Acknowledgements

I am thankful to numerous stingless bee enthusiasts and admirers, most of all Nico Blüthgen, who introduced me to their fascinating world, and to Thomas Schmitt for sharing his excitement about their chemical ecology. I am further grateful for the helpful comments of two reviewers. My own research on stingless bee chemical ecology was funded by a grant of the German Excellence Initiative to the Graduate School of Life Science, University of Würzburg, and by the Deutsche Forschungsgemeinschaft (DFG project: LE 2750/1-1).

References

  1. Abdalla FC, Jones GR, Morgan ED, Da Cruz-Landim C (2003) Comparative study of the cuticular hydrocarbon composition of Melipona bicolor Lepeletier, 1836 (Hymenoptera, Meliponini) workers and queens. Genet Mol Res 2(2):191–199PubMedGoogle Scholar
  2. Afik O, Delaplane KS, Shafir S, Moo-Valle H, Quezada-Euán JJG (2014) Nectar minerals as regulators of flower visitation in stingless bees and nectar hoarding wasps. J Chem Ecol 40:476–483PubMedCrossRefGoogle Scholar
  3. Aguilar I, Fonseca A, Biesmeijer JC (2005) Recruitment and communication of food source location in three species of stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 36:313–324CrossRefGoogle Scholar
  4. Bartareau T (1996) Foraging behaviour of Trigona carbonaria (Hymenoptera: Apidae) at multiple-choice feeding stations. Aust J Zool 44:143–153CrossRefGoogle Scholar
  5. Barth FG, Hrncir M, Jarau S (2008) Signals and cues in the recruitment behavior of stingless bees (Meliponini). Journal of Comparative Physiology a-Neuroethology Sensory Neural and Behavioral Physiology 194(4):313–327CrossRefGoogle Scholar
  6. Biesmeijer JC, Ermers M (1999a) Social foraging in stingless bees: how colonies of Melipona fasciata choose among nectar sources. Behav Ecol Sociobiol 46(2):129–140CrossRefGoogle Scholar
  7. Biesmeijer JC, Richter JP, Smeets M, Sommeijer MJ (1999b) Niche differentiation in nectar-collecting stingless bees: the influence of morphology, floral choice and interference competition. Ecol Entomol 24(4):380–388CrossRefGoogle Scholar
  8. 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(8):1637–1648PubMedCrossRefGoogle Scholar
  9. Bowden RM, Garry MF, Breed MD (1994) Discrimination of conspecific and heterospecific bees by Trigona (Tetragonisca) angustula guards. J Kansas Entomol Soc 67(1):137–139Google Scholar
  10. Breed MD, Garry MF, Pearce AN, Hibbard BE, Bjostad LB, Page RE (1995) The role of wax comb in honeybee nestmate recognition. Anim Behav 50:489–496CrossRefGoogle Scholar
  11. Breed MD, Page RE (1991) Intraspecific and interspecific nestmate recognition in Melipona workers (Hymenoptera, Apidae). J Insect Behav 4(4):463–469CrossRefGoogle Scholar
  12. Breed MD, Perry S, Bjostad LB (2004) Testing the blank slate hypothesis: why honeybee colonies accept young bees. Insect Soc 51:12–16CrossRefGoogle Scholar
  13. Buchwald R, Breed MD (2005) Nestmate recognition cues in a stingless bee, Trigona fulviventris. Anim Behav 70:1331–1337CrossRefGoogle Scholar
  14. Caliari Oliveira R, Oi CA, Castro Do Nascimento MM, Vollet-Neto A, Alves DA, Campos MC, Nascimento F, Wenseleers T (2015) The origin and evolution of queen and fertility signals in Corbiculate bees. BMC Evol Biol 15:254PubMedPubMedCentralCrossRefGoogle Scholar
  15. Cardinal S, Straka J, Danforth BN (2010) Comprehensive phylogeny of apid bees reveals the evolutionary origins and antiquity of cleptoparasitism. Proc Natl Acad Sci U S A 107:16207–16211PubMedPubMedCentralCrossRefGoogle Scholar
  16. Celemli ÖG (2013) Chemical properties of propolis collected by stingless bees. In: Vit P, Pedro SRM, Roubik D (eds) Pot-honey: a legacy of stingless bees. Springer, New York, pp 525–537CrossRefGoogle Scholar
  17. Couvillon MJ, Ratnieks FLW (2009) 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
  18. 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(1):43–47CrossRefGoogle Scholar
  19. 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(7):1621–1632PubMedCrossRefGoogle Scholar
  20. Da Silva GR, Da Natividade TB, Camara CA, Sarmento Da Silva EM, Dos Santos FDaR, Sarmento Silva TM (2014) Identification of sugar, amino acids and minerals from the pollen of Jandaíra stingless bees (Melipona subnitida). Food Nutr Sci 5:1015–1021Google Scholar
  21. Dambacher J, Jarau S, Twele R, Aguilar I, Francke W, Ayasse M. (2007) Nest specific information in the trail pheromone of a stingless bee, Trigona corvina (Hymenoptera, Apidae, Meliponini). Jena, Germany, p 248Google Scholar
  22. Drescher N, Wallace HM, Katouli M, Massaro CF, Leonhardt SD (2014) Diversity matters: how bees benefit from different resin sources. Oecologia 176(4):943–953PubMedCrossRefGoogle Scholar
  23. Duangphakdee O, Koeniger N, Deowanish S, Hepburn HR, Wongsiri S (2009) Ant repellent resins of honeybees and stingless bees. Insect SocGoogle Scholar
  24. Dworschak (2006) Interactions between stingless bees (Hymeoptera: Apidae: Meliponini). Julius-Maximilians-Universität Würzburg, Würzburg, 51 pGoogle Scholar
  25. Dworschak K, Blüthgen N (2010) Networks and dominance hierarchies: does interspecific aggression explain flower partitioning among stingless bees? Ecol Entomol 35(2):216–225CrossRefGoogle Scholar
  26. Engels E, Engels W (1984) Drone aggregations near the nest of the stingless bee, Scaptotrigona postica. Apidologie 15(3):315–328CrossRefGoogle Scholar
  27. Engels E, Engels W (1988) Age-dependent queen attractiveness for drones and mating in the stingless bee Scaptotrigona postica. Journal of Apicultural Research and Bee World 27(1)Google Scholar
  28. Engels W, Engels E, Francke W (1997) Ontogeny of cephalic volatile patterns in queens and mating biology of the neotropical stingless bee, Scaptotrigona postica. Invertebr Reprod Dev 31(1–3):251–256CrossRefGoogle Scholar
  29. Engels W, Engels E, Lubke G, Schroder W, Francke W (1990) Volatile cephalic secretions of drones, queens and workers in relation to reproduction in the stingless bee, Scaptotrigon postica (Hymenoptera, Apidae, Trigonini). Entomol Gen 15(2):91–101CrossRefGoogle Scholar
  30. Engels E, Engels W, Lubke G, Schroder W, Francke W (1993) Age-related patterns of volatile cephalic constituents in queens of the Neotropical stingless bee Scaptotrigona postica Latr (Hymenoptera, Apidae). Apidologie 24(6):539–548CrossRefGoogle Scholar
  31. 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(2):371–386PubMedCrossRefGoogle Scholar
  32. Ferreira-Caliman MJ, Da Silva CI, Mateus S, Zucchi R, Nascimento FS (2012b) Neutral sterols of cephalic glands of stingless bees and their correlation with sterols from pollen. Psyche 2012Google Scholar
  33. Ferreira-Caliman MJ, Falcón T, Mateus S, Zucchi R, Nascimento FS (2013) Chemical identity of recently emerged workers, males, and queens in the stingless bee Melipona marginata. Apidologie 44(6):657–665CrossRefGoogle Scholar
  34. Ferreira-Caliman MJ, Nascimento FS, Turatti IC, Mateus S, Lopes NP, Zucchi R (2010) The cuticular hydrocarbons profiles in the stingless bee Melipona marginata reflect task-related differences. J Insect Physiol 56:800–804PubMedCrossRefGoogle Scholar
  35. Ferreira-Caliman MJ, Nascimento FS, Zucchi R (2012a) First record of chemical signals from the queen during the oviposition process in stingless bees. Insect Soc 59:599–600CrossRefGoogle Scholar
  36. 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 37:1255–1262PubMedCrossRefGoogle Scholar
  37. Gardener MC, Rowe RJ, Gillman MP (2003) Tropical bees (Trigona hockingsi) show no preference for nectar with amino acids. Biotropica 35(1):119–125Google Scholar
  38. Greco MK, Hoffmann D, Dollin A, Duncan M, Spooner-Hart R, Neumann P (2010) The alternative pharao approach: stingless bees mummify beetle parasites alive. Naturwissenschaften 97(3):319–323PubMedCrossRefGoogle Scholar
  39. Grüter C, Von Zuben LG, Segers FHID, Cunningham JP (2016) Warfare in stingless bees. Insect Soc 63(2):223–236CrossRefGoogle Scholar
  40. Gutiérrez E, Ruiz D, Solís T, May-Itzá WDJ, Moo-Valle H, Quezada-Euan JJG (2016) Does larval food affect cuticular profiles and recognition in eusocial bees? A test on Scaptotrigona gynes (Hymenoptera: Meliponini). Behav Ecol Sociobiol 70:871–879CrossRefGoogle Scholar
  41. Halcroft M, Spooner-Hart R, Neumann P (2011) Behavioral defense strategies of the stingless bee, Austroplebeia australis, against the small hive beetle. Insect Soc 58(2):245–253CrossRefGoogle Scholar
  42. Hanus R, Vrkoslav V, Hrdý I, Cvačka J, Šobotník J (2010) Beyond cuticular hydrocarbons: evidence of proteinaceous secretion specific to termite kings and queens. Proc R Soc B Biol Sci 277:995–1002CrossRefGoogle Scholar
  43. Hartfelder K, Engels W (1989) The composition of larval food in stingless bees: evaluating nutritional balance by chemosystematic methods. Insect Soc 36:1–14CrossRefGoogle Scholar
  44. Heard TA (1999) The role of stingless bees in crop pollination. Annu Rev Entomol 44:183–206PubMedCrossRefGoogle Scholar
  45. Heard TA (2016) The Australian native bee book. Keeping stingless bee hives for pets, pollination and sugarbag honey. Sugarbag Bees, BrisbaneGoogle Scholar
  46. Howard JJ (1985) Observations on resin collecting by six interacting species of stingless bees (Apidae, Meliponinae). J Kansas Entomol Soc 58(2):337–345Google Scholar
  47. Hrncir M, Jarau S, Barth FG (2016) Stingless bees (Meliponini): senses and behavior (editorial). J Comp Physiol A 202:597–601CrossRefGoogle Scholar
  48. Hubbell SP, Johnson LK (1978) Comparative foraging behavior of six stingless bee species exploiting a standardized resource. Ecology 59(6):1123–1136CrossRefGoogle Scholar
  49. Inoue T, Roubik DW (1990) Kin recognition of the stingless bee Melipona fasciata. In: Veeresh GK, Mallik R, Viraktamath CA (eds) Social insects and the environment. Oxford & IBH Publishing Co, New Delhi, pp 517–518Google Scholar
  50. Inoue T, Roubik DW, Suka T (1999) Nestmate recognition in the stingless bee Melipona panamica (Apidae, Meliponini). Insect Soc 46(3):208–218CrossRefGoogle Scholar
  51. Jarau S (2009) Chemical communication during food exploitation in stingless bees, pp 223–249Google Scholar
  52. Jarau S, Hrncir M, Ayasse M, Schulz C, Francke W, Zucchi R, Barth FG (2004) A stingless bee marks food sources with a pheromone from its claw retractor tendons. J Chem Ecol 30:793–804PubMedCrossRefGoogle Scholar
  53. Jarau S, Schulz C, 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 32:1555–1564PubMedCrossRefGoogle Scholar
  54. Jarau S, Van Veen JW, Twele R, Reichle C, Herrera Gonzales E, Aguilar I, Francke W, Ayasse M (2010) Workers make the queens in Melipona bees: identification of geraniol as a caste determining compound from labial glands of nurse bees. J Chem Ecol 36:565–569PubMedCrossRefGoogle Scholar
  55. John L, Aguilar I, Ayasse M, Jarau S (2012) Nest-specific composition of the trail pheromone of the stingless bee Trigona corvina within populations. Insect Soc 59(4):527–532CrossRefGoogle Scholar
  56. Johnson LK, Haynes LW, Carlson MA, Fortnum HA, Gorgas DL (1985) Alarm substances of the stingless bee Trigona sylvestriana. J Chem Ecol 11:409–416PubMedCrossRefGoogle Scholar
  57. Johnson LK, Hubbell SP (1974) Aggression and competition among stingless bees - field studies. Ecology 55(1):120–127CrossRefGoogle Scholar
  58. Johnson LK, Wiemer DF (1982) Nerol: an alarm substance of the stingless bee Trigona fulviventris (Hymenoptera: Apidae). J Chem Ecol 8(9):1167–1181PubMedCrossRefGoogle Scholar
  59. Jones SM, Van Zweden JS, Christoph 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
  60. Jungnickel H, Da Costa AJS, Tentschert J, Patricio E, 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(8):761–766PubMedCrossRefGoogle Scholar
  61. Kather R, Drijfhout FP, Martin SJ (2011) Task group differences in cuticular lipids in the honey bee Apis mellifera. J Chem Ecol 37:205–212PubMedCrossRefGoogle Scholar
  62. Keller L, Nonacs P (1993) The role of queen pheromones in social insects: queen control or queen signal? Anim Behav 45:787–794CrossRefGoogle Scholar
  63. Kerr WE, Jungnickel H, Morgan ED (2004) Workers of the stingless bee Melipona scutellaris are more similar to males than to queens in their cuticular compounds. Apidologie 35(6):611–618CrossRefGoogle Scholar
  64. Kerr WE, Zucchi R, Nakadaira JT, Botolo JD (1962) Reproduction in the social bees (Hymenoptera: Apidae). Journal of the New York Entomological Society 70:265–276Google Scholar
  65. Khoo SG, Yong HS (1987) Nest structure and colony defense in the stingless bee Trigona terminata Smith. Nature Malaysiana 12:4–15Google Scholar
  66. Kirchner WH, Friebe R (1999) Nestmate discrimination in the African stingless bee Hypotrigona gribodoi Magretti (Hymenoptera: Apidae). Apidologie 30(4):293–298CrossRefGoogle Scholar
  67. Langenheim JH (2003) Plant resins: chemistry, evolution, ecology and ethnobotany. Timber Press, Portland, p 586Google Scholar
  68. Lehmberg L, Dworschak K, Blüthgen N (2008) Defensive behavior and chemical deterrence against ants in the stingless bee genus Trigona (Apidae, Meliponini). J Apic Res 47:17–21CrossRefGoogle Scholar
  69. Leonhardt SD, Baumann A-M, Wallace HM, Brooks P, Schmitt T (2014) The chemistry of an unusual seed disperal mutualism: bees use a complex set of chemical cues to find their partner. Anim Behav 98:41–51CrossRefGoogle Scholar
  70. Leonhardt SD, Blüthgen N (2009a) A sticky affair: resin collection by Bornean stingless bees. Biotropica 41(6):730–736CrossRefGoogle Scholar
  71. Leonhardt SD, Blüthgen N, Schmitt T (2009b) Smelling like resin: terpenoids account for species-specific cuticular profiles in southeast-Asian stingless bees. Insect Soc 56:157–170CrossRefGoogle Scholar
  72. Leonhardt SD, Blüthgen N, Schmitt T (2010a) Chemical profiles of body surfaces and nests from six Bornean stingless bee species. J Chem Ecol 37:98–104PubMedCrossRefGoogle Scholar
  73. Leonhardt SD, Jung L-M, Schmitt T, Blüthgen N (2010c) Terpenoids tame aggressors: role of chemicals in stingless bee communal nesting. Behav Ecol Sociobiol 64:1415–1423CrossRefGoogle Scholar
  74. Leonhardt SD, Menzel F, Nehring V, Schmitt T (2016) Ecology and evolution of communication in social insects. Cell 164(6):1277–1287PubMedCrossRefGoogle Scholar
  75. Leonhardt SD, Rasmussen C, Schmitt T (2013) Genes vs. environment: Geography and phylogenetic relationships shape the chemical profiles of stingless bees on a global scale. Proc R Soc Lond B 280(1762):20130680CrossRefGoogle Scholar
  76. Leonhardt SD, Schmitt T, Blüthgen N (2011a) Tree resin composition, collection behavior and selective filters shape chemical profiles of tropical bees (Apidae: Meliponini). PLoS One 6(8):e23445PubMedPubMedCentralCrossRefGoogle Scholar
  77. Leonhardt SD, Wallace HM, Blüthgen N, Wenzel F (2015) Potential role of environmentally derived cuticular compounds in stingless bees. Chemoecology (in press)Google Scholar
  78. Leonhardt SD, Wallace HM, Schmitt T (2011b) The cuticular profiles of Australian stingless bees are shaped by resin of the eucalypt tree Corymbia torelliana. Austral Ecology 36:537–543CrossRefGoogle Scholar
  79. Leonhardt SD, Zeilhofer S, Schmitt T (2010b) Stingless bees use terpenes as olfactory cues to find resin sources. Chem Senses 35:603–611PubMedCrossRefGoogle Scholar
  80. Lichtenberg EM, Hrncir M, Turatti IC, Nieh JC (2011) Olfactory eavesdropping between two competing stingless bee species. Behav Ecol Sociobiol 65(4):763–774PubMedCrossRefGoogle Scholar
  81. Lindauer M (1956) Über die Verständigung bei indischen Bienen. Z Vergl Phys 38:521–557CrossRefGoogle Scholar
  82. Lindauer M, Kerr WE (1958) Die gegenseitige Verständigung bei den stachellosen Bienen. Z Vergl Phys 41(4):405–434CrossRefGoogle Scholar
  83. Lindauer M, Kerr WE (1960) Communication between the workers of stingless bees. Bee World 41:29–41CrossRefGoogle Scholar
  84. Litman JR, Danforth BN, Eardley CD, Praz CJ (2011) Why do leafcutter bees cut leaves? New insights into the early evolution of bees. Proc R Soc Lond B 278:3593–3600CrossRefGoogle Scholar
  85. Luby JM, Regnier FE, Clarke ET, Weaver EC, Weaver N (1973) Volatile cephalic substances of the stingless bees Trigona mexicana and Trigona pectoralis. J Insect Physiol 19:1111–1127CrossRefGoogle Scholar
  86. Massaro CF, Katouli M, Grkovic T, Vu H, Quinn RJ, Heard TA, Carvalho C, Manley-Harris M, Wallace HM, Brooks P (2014b) Anti-staphylococcal activity of C-methyl flavanones from propolis of Australian stingless bees (Tetragonula carbonaria) and fruit resins of Corymbia torelliana (Myrtaceae). Fitoterapia 95:247–257PubMedCrossRefGoogle Scholar
  87. Massaro CF, Smyth TJ, Smyth WF, Heard T, Leonhardt SD, Katouli M, Wallace HM, Brooks P (2014a) Phloroglucinols from anti-microbial deposit-resins of Australian stingless bees (Tetragonula carbonaria). Phytother ResGoogle Scholar
  88. Mc Cabe SI, Farina WM (2010) Olfactory learning in the stingless bee Tetragonisca angustula (Hymenoptera, Apidae, Meliponini). J Comp Physiol A 196(7):481–490CrossRefGoogle Scholar
  89. Michener CD (1974) The social behavior of the bees. Belknap Press of Harvard University Press, Cambridge, p 404Google Scholar
  90. Michener CD (1979) Biogeography of the bees. Ann Mo Bot Gard 66(3):277–347CrossRefGoogle Scholar
  91. Michener CD (2007) The bees of the world. John Hopkins University Press, Baltimore, London, p 953Google Scholar
  92. Nagamitsu T, Inoue T (1997) Aggressive foraging of social bees as a mechanism of floral resource partitioning in an Asian tropical rainforest. Oecologia 110(3):432–439PubMedCrossRefGoogle Scholar
  93. 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 38:1432–1440PubMedCrossRefGoogle Scholar
  94. Nicolson SW (2011) Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two. Afr Zool 46(2):197–204CrossRefGoogle Scholar
  95. Nieh JC (2004) Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 35:159–182CrossRefGoogle Scholar
  96. Nieh JC, Tautz J, Spaethe J, Bartareau T (2000) The communication of food location by a primitive stingless bee, Trigona carbonaria. Zoology 102(239–246)Google Scholar
  97. 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 (2014b) Queen signals in a stingless bee: suppression of worker ovary activation and spatial distribution of active compounds. Sci Rep 4:7449PubMedPubMedCentralCrossRefGoogle Scholar
  98. Nunes TM, Mateus S, Turatti IC, Morgan ED, Zucchi R (2011) Nestmate recognition in the stingless bee Frieseomelitta varia (Hymenoptera, Apidae, Meliponini): sources of chemical signals. Anim Behav 81:463–467CrossRefGoogle Scholar
  99. Nunes TM, Morgan ED, Drijfhout FP, Zucchi R (2010) Caste-specific cuticular lipids in the stingless bee Friesella schrottkyi. Apidologie 41:579–588CrossRefGoogle Scholar
  100. 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
  101. Nunes TM, Turatti ICC, Lopes NP, Zucchi R (2009a) Chemical signals in the stingless bee, Frieseomelitta varia, indicate caste, gender, age, and reproductive status. J Chem Ecol 35(10):1172–1180PubMedCrossRefGoogle Scholar
  102. Nunes TM, Turatti ICC, 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(2):589–595PubMedCrossRefGoogle Scholar
  103. Nunes TM, Von Zuben LG, Costa L, Venturieri GC (2014a) Defensive repertoire of the stingless bee Melipona flavolineata Friese (Hymenoptera: Apidae). Sociobiology 61(4):541–546CrossRefGoogle Scholar
  104. Paxton RJ, Weißschuh N, Engels W, Hartfelder K, Quezada-Euan JJG (1999) Not only single mating in stingless bees. Naturwissenschaften 86:143–146CrossRefGoogle Scholar
  105. Peters JM, Queller DC, Imperatriz-Fonseca VL, Roubik DW, Strassmann JE (1999) Mate number, kin selection and social conflicts in stingless bees and honeybees. Proc R Soc B Biol Sci 266:379–384CrossRefGoogle Scholar
  106. 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 40:331–340PubMedCrossRefGoogle Scholar
  107. 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(4):817–823CrossRefGoogle Scholar
  108. 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
  109. Rebelo KS, Ferreira AG, Carvalho-Zilse GA (2016) Physicochemical characteristics of pollen collected by Amazonian stingless bees. Ciência Rural, Santa Maria 46(5):927–932CrossRefGoogle Scholar
  110. Reichle C, Aguilar I, Ayasse M, Jarau S (2011) Stingless bees (Scaptotrigona pectoralis) learn foreign trail pheromones and use them to find food. J Comp Physiol A 197(3):243–249CrossRefGoogle Scholar
  111. Reichle C, Aguilar I, Ayasse M, Twele R, Francke W, Jarau S (2013) Learnt information in species-specific ‘trail pheromone’ communication in stingless bees. Anim Behav 85(1):225–232CrossRefGoogle Scholar
  112. Reichle C, Jarau S, Aguilar I, Ayasse M (2010) Recruits of the stingless bee Scaptotrigona pectoralis learn food odors from the nest atmosphere. Naturwissenschaften 97(5):519–524PubMedCrossRefGoogle Scholar
  113. Rinderer TE, Blum MS, Fales HM, Bian Z, Jones TH, Buco SM, Lancaster VA, Danka RG, Howard DF (1988) Nest plundering allomones of the fire bee Trigona (Oxytrigona) mellicolor. J Chem Ecol 14:495–501PubMedCrossRefGoogle Scholar
  114. Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, New York, p 514CrossRefGoogle Scholar
  115. Roubik DW (2006) Stingless bee nesting biology. Apidologie 37(2):124–143CrossRefGoogle Scholar
  116. Roubik DW, Buchmann SL (1984) Nectar selection by Melipona and Apis mellifera (Hymenoptera: Apidae) and the ecology of nectar intake by bee colonies in a tropical forest. Oecologia 61:1–10PubMedCrossRefGoogle Scholar
  117. Roubik DW, Yanega D, Aluja M, Buchmann SL, Inouye DW (1995) On optimal nectar foraging by some tropical bees (Hymenoptera, Apidae). Apidologie 26:197–211CrossRefGoogle Scholar
  118. Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. Plant Syst Evol 222(1–4):187–209CrossRefGoogle Scholar
  119. Santa Bárbara M, Santiago Machado C, Da Silva SG, Dias LG, Estevinho LM, Lopes De Carvalho CA (2015) Microbiological assessment, nutritional characterization and phenolic compounds of bee pollen from Melipona mandacaia Smith, 1983. Molecules 20:12525–12544CrossRefGoogle Scholar
  120. Sarmento Silva TM, Camara CA, Da Silva Linsa AC, Barbosa-Filhoa JM, Sarmento Da Silva EM, Freitas BM, Dos Santos FDR (2006) Chemical composition and free radical scavenging activity of pollen loads from stingless bee Melipona subnitida Ducke. J Food Compos Anal 19:507–511CrossRefGoogle Scholar
  121. 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(8):1153–1162PubMedCrossRefGoogle Scholar
  122. Schorkopf DL, Jarau S, Franke 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 Biol Sci 274:895–898CrossRefGoogle Scholar
  123. Schwarz HF (1948) Stingless bees of the western hemisphere. Bull Am Mus Nat Hist 90:1–546Google Scholar
  124. Septanil MB, Mateus S, Turatti IC, 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
  125. Shackleton K, Al Toufailia H, Balfour NJ, Nascimento 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(2):273–281PubMedCrossRefGoogle Scholar
  126. Silva TMS, Camara CA, Lins ACS, Agra MDF, Silva EMS, Reis IT, Freitas BM (2009) Chemical composition, botanical evaluation and screening of radical scavenging activity of collected pollen by the stingless bees Melipona rufiventris (Uruçu-amarela). Annals of the Brazilian Academy of Sciences 81(2):173–178CrossRefGoogle Scholar
  127. Simone M, Evans JD, Spivak M (2009) Resin collection and social immunity in honey bees. Evolution 63(11):3016–3022PubMedCrossRefGoogle Scholar
  128. Simone-Finstrom M, Spivak M (2010) Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41(3):295–311CrossRefGoogle Scholar
  129. Simpson SJ, Raubenheimer D (2012) The nature of nutrition: a unifying framework from animal adaptation to human obesity. Princeton University Press, PrincetonCrossRefGoogle Scholar
  130. Slaa EJ, Cevaal A, Sommeijer MJ (1998) Floral constancy in Trigona stingless bees foraging on artificial flower patches: a comparative study. Journal of Apicultural Research and Bee World 37:191–198CrossRefGoogle Scholar
  131. Slaa EJ, Tack AJM, Sommeijer MJ (2003) The effect of intrinsic and extrinsic factors on flower constancy in stingless bees. Apidologie 34:457–468CrossRefGoogle Scholar
  132. 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(11):1465–1472PubMedCrossRefGoogle Scholar
  133. Sommeijer JM, De Bruijn LLM (1995) Drone congregations apart from the nest in Melipona favosa. Insect Soc 42:123–127CrossRefGoogle Scholar
  134. Sommeijer JM, De Bruijn MLL, Meeuwsen JFJA, Martens PE (2003) Natural patterns of caste and sex allocation in the stingless bees Melipona favosa and M. trinitatis related to worker behaviour. Insect Soc 50(1):38–44CrossRefGoogle Scholar
  135. Souza RCS, Yuyama LKO, Aguiar JPL, Oliveira FPM (2004) Valor nutricional do mel e pólen de abelhas sem ferrão da região amazônica. Acta Amazon 34:333–336CrossRefGoogle Scholar
  136. Stangler ES, Jarau S, Hrncir M, Zucchi R, Ayasse M (2009) Identification of trail pheromone compounds from the labial glands of the stingless bee Geotrigona mombuca. Chemoecology 19(1):13–19CrossRefGoogle Scholar
  137. Suka T, Inoue T (1993) Nestmate recognition of the stingless bee Trigona (Tetragonula) minangkabau (Apidae, Meliponinae). J Ethol 11(2):141–147CrossRefGoogle Scholar
  138. Suka T, Inoue T, Roubik DW (1994) Worker oviposition and kin recognition of the stingless bee Scaptotrigona barrocoloradensis. In: Lenoir A, Arnold G, Lepage M (eds) Les Insectes Sociaux. Universite Paris Nord, Villetaneuse, p 338Google Scholar
  139. Turillazzi S, Mastrobuoni G, Dani FR, Moneti G, Pieraccini G, La Marca G, Bartolucci G, Perito B, Lambardi D, Cavallini V (2006) Dominulin a and B: two new antibacterial peptides identified on the cuticle and in the venom of the social paper wasp Polistes dominulus using MALDI-TOF, MALDITOF/TOF, and ESI-ion trap. J Am Soc Mass Spectrom 17:376–383PubMedCrossRefGoogle Scholar
  140. Van Oystaeyen A, Oliveira RC, Holman L, Van Zweden JS, Romero C, Oi CA, D’ettorre P, Khalesi M, Billen J, Wäckers F, Millar JG, Wenseleers T (2014) Conserved class of queen pheromones stops social insect workers from reproducing. Science 343:287–290PubMedCrossRefGoogle Scholar
  141. Van Veen WJ, Sommeijer JM (2000) Colony reproduction in Tetragonisca angustula (Apidae, Meliponini). Insect Soc 47(1):70–75CrossRefGoogle Scholar
  142. Van Veen JW, Sommeijer MJ, Meeuwsen JFJA (1997) Behaviour of drones in Melipona (Apidae, Meliponinae). Insect Soc 44:435–447CrossRefGoogle Scholar
  143. Vaudo AD, Tooker JF, Grozinger CM, Patch HM (2015) Bee nutrition and floral resource restoration. Current Opinion in Insect Science 10:133–141CrossRefGoogle Scholar
  144. Velikova M, Bankova V, Marcucci MC, Tsvetkova I, Kujumgiev A (2000a) Chemical composition and biological activity of propolis from Brazilian Meliponinae. Z Naturforsch C 55(9–10):785–789PubMedGoogle Scholar
  145. Velikova M, Bankova V, Tsvetkova I, Kujumgiev A, Marcucci MC (2000b) Antibacterial ent-kaurene from Brazilian propolis of native stingless bees. Fitoterapia 71(6):693–696PubMedCrossRefGoogle Scholar
  146. Verdugo-Dardon M, Cruz-Lopez L, Malo E, Rojas J, Guzman-Diaz M (2011) Olfactory attraction of Scaptotrigona mexicana drones to their virgin queen volatiles. Apidologie 42(4):543–550CrossRefGoogle Scholar
  147. Vit P, Pedro SRM, Roubik D (2013) Pot-honey: a legacy of stingless bees. Springer, New YorkCrossRefGoogle Scholar
  148. Von Frisch K (1967) The dance language and orientation of bees. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  149. Von Ihering H (1886) Der Stachel der Meliponen. Entomologische Nachrichten 12:177–188Google Scholar
  150. 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
  151. Wallace HM, Howell MG, Lee DJ (2008) Standard yet unusual mechanisms of long-distance dispersal: seed dispersal of Corymbia torelliana by bees. Divers Distrib 14(1):87–94CrossRefGoogle Scholar
  152. Wallace HM, Lee DJ (2010) Resin-foraging by colonies of Trigona sapiens and T. hockingsi (Hymenoptera: Apidae, Meliponini) and consequent seed dispersal of Corymbia torelliana (Myrtaceae). Apidologie 41:428–435CrossRefGoogle Scholar
  153. Wallace HM, Trueman SJ (1995) Dispersal of Eucalyptus torelliana seeds by the resin-collecting stingless bee, Trigona carbonaria. Oecologia 104(1):12–16PubMedCrossRefGoogle Scholar
  154. Weaver N, Weaver EC, Clarke ET (1975) Reactions of five species of stingless bees to some volatile chemicals and to other species of bees. J Insect Physiol 21(3):479–494CrossRefGoogle Scholar
  155. Wille A (1983) Biology of the stingless bee. Annu Rev Entomol 28:41–46CrossRefGoogle Scholar
  156. Wilson EO (1971) The insect societies. Belknap Press of the Harvard University Press, pp 560Google Scholar
  157. Wilson MB, Spivak M, Hegeman AD, Rendahl A, Cohen JD (2013) Metabolomics reveals the origins of antimicrobial plant resins collected by honey bees. PLoS One 8(10):e77512PubMedPubMedCentralCrossRefGoogle Scholar
  158. Wittmann D (1985) Aerial defense of the nest by workers of the stingless bee Trigona (Tetragonisca) angustula (Latreille) (Hymenoptera, Apidae). Behav Ecol Sociobiol 16(2):111–114CrossRefGoogle Scholar
  159. Wittmann D, Radtke R, Zeil J, Lubke G, Francke W (1990) Robber bees (Lestrimelitta limao) and their host chemical and visual cues in nest defense by Trigona (Tetragonisca) angustula (Apidae, Meliponinae). J Chem Ecol 16(2):631–641PubMedCrossRefGoogle Scholar
  160. Zupko K, Sklan D, Lensky Y (1993) Proteins of the honeybee (Apis mellifera L.) body surface and exocrine gland secretions. J Insect Physiol 39:41–46CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Department of Animal Ecology and Tropical BiologyUniversity of WürzburgWürzburgGermany

Personalised recommendations