Skip to main content
Log in

Chemical Ecology of Stingless Bees

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • 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):191–199

    CAS  PubMed  Google Scholar 

  • 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 40:476–483

    Article  CAS  PubMed  Google Scholar 

  • Aguilar I, Fonseca A, Biesmeijer JC (2005) Recruitment and communication of food source location in three species of stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 36:313–324

    Article  Google Scholar 

  • Bartareau T (1996) Foraging behaviour of Trigona carbonaria (Hymenoptera: Apidae) at multiple-choice feeding stations. Aust J Zool 44:143–153

    Article  Google Scholar 

  • 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):313–327

    Article  Google Scholar 

  • Biesmeijer JC, Ermers M (1999a) Social foraging in stingless bees: how colonies of Melipona fasciata choose among nectar sources. Behav Ecol Sociobiol 46(2):129–140

    Article  Google Scholar 

  • 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):380–388

    Article  Google Scholar 

  • 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):1637–1648

    Article  CAS  PubMed  Google Scholar 

  • Bowden RM, Garry MF, Breed MD (1994) Discrimination of conspecific and heterospecific bees by Trigona (Tetragonisca) angustula guards. J Kansas Entomol Soc 67(1):137–139

    Google Scholar 

  • Breed MD, Garry MF, Pearce AN, Hibbard BE, Bjostad LB, Page RE (1995) The role of wax comb in honeybee nestmate recognition. Anim Behav 50:489–496

    Article  Google Scholar 

  • Breed MD, Page RE (1991) Intraspecific and interspecific nestmate recognition in Melipona workers (Hymenoptera, Apidae). J Insect Behav 4(4):463–469

    Article  Google Scholar 

  • Breed MD, Perry S, Bjostad LB (2004) Testing the blank slate hypothesis: why honeybee colonies accept young bees. Insect Soc 51:12–16

    Article  Google Scholar 

  • Buchwald R, Breed MD (2005) Nestmate recognition cues in a stingless bee, Trigona fulviventris. Anim Behav 70:1331–1337

    Article  Google Scholar 

  • 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 15:254

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 107:16207–16211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 525–537

    Chapter  Google Scholar 

  • 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 62:1099–1105

    Article  Google Scholar 

  • 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):43–47

    Article  CAS  Google Scholar 

  • 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):1621–1632

    Article  CAS  PubMed  Google Scholar 

  • 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 5:1015–1021

  • 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 248

  • Drescher N, Wallace HM, Katouli M, Massaro CF, Leonhardt SD (2014) Diversity matters: how bees benefit from different resin sources. Oecologia 176(4):943–953

    Article  PubMed  Google Scholar 

  • Duangphakdee O, Koeniger N, Deowanish S, Hepburn HR, Wongsiri S (2009) Ant repellent resins of honeybees and stingless bees. Insect Soc

  • Dworschak (2006) Interactions between stingless bees (Hymeoptera: Apidae: Meliponini). Julius-Maximilians-Universität Würzburg, Würzburg, 51 p

    Google Scholar 

  • Dworschak K, Blüthgen N (2010) Networks and dominance hierarchies: does interspecific aggression explain flower partitioning among stingless bees? Ecol Entomol 35(2):216–225

    Article  Google Scholar 

  • Engels E, Engels W (1984) Drone aggregations near the nest of the stingless bee, Scaptotrigona postica. Apidologie 15(3):315–328

    Article  Google Scholar 

  • 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)

  • 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):251–256

    Article  CAS  Google Scholar 

  • 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):91–101

    Article  Google Scholar 

  • 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):539–548

    Article  CAS  Google Scholar 

  • 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):371–386

    Article  CAS  PubMed  Google Scholar 

  • 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 2012

  • 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):657–665

    Article  CAS  Google Scholar 

  • 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 56:800–804

    Article  CAS  PubMed  Google Scholar 

  • 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 59:599–600

    Article  Google Scholar 

  • 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 37:1255–1262

    Article  CAS  PubMed  Google Scholar 

  • Gardener MC, Rowe RJ, Gillman MP (2003) Tropical bees (Trigona hockingsi) show no preference for nectar with amino acids. Biotropica 35(1):119–125

    Google Scholar 

  • 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):319–323

    Article  CAS  PubMed  Google Scholar 

  • Grüter C, Von Zuben LG, Segers FHID, Cunningham JP (2016) Warfare in stingless bees. Insect Soc 63(2):223–236

    Article  Google Scholar 

  • 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 70:871–879

    Article  Google Scholar 

  • 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):245–253

    Article  Google Scholar 

  • 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 277:995–1002

    Article  CAS  Google Scholar 

  • Hartfelder K, Engels W (1989) The composition of larval food in stingless bees: evaluating nutritional balance by chemosystematic methods. Insect Soc 36:1–14

    Article  Google Scholar 

  • Heard TA (1999) The role of stingless bees in crop pollination. Annu Rev Entomol 44:183–206

    Article  CAS  PubMed  Google Scholar 

  • Heard TA (2016) The Australian native bee book. Keeping stingless bee hives for pets, pollination and sugarbag honey. Sugarbag Bees, Brisbane

    Google Scholar 

  • Howard JJ (1985) Observations on resin collecting by six interacting species of stingless bees (Apidae, Meliponinae). J Kansas Entomol Soc 58(2):337–345

    Google Scholar 

  • Hrncir M, Jarau S, Barth FG (2016) Stingless bees (Meliponini): senses and behavior (editorial). J Comp Physiol A 202:597–601

    Article  Google Scholar 

  • Hubbell SP, Johnson LK (1978) Comparative foraging behavior of six stingless bee species exploiting a standardized resource. Ecology 59(6):1123–1136

    Article  Google Scholar 

  • 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 517–518

    Google Scholar 

  • Inoue T, Roubik DW, Suka T (1999) Nestmate recognition in the stingless bee Melipona panamica (Apidae, Meliponini). Insect Soc 46(3):208–218

    Article  Google Scholar 

  • Jarau S (2009) Chemical communication during food exploitation in stingless bees, pp 223–249

  • 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 30:793–804

    Article  CAS  PubMed  Google Scholar 

  • 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 32:1555–1564

    Article  CAS  PubMed  Google Scholar 

  • 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 36:565–569

    Article  CAS  PubMed  Google Scholar 

  • 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):527–532

    Article  Google Scholar 

  • Johnson LK, Haynes LW, Carlson MA, Fortnum HA, Gorgas DL (1985) Alarm substances of the stingless bee Trigona sylvestriana. J Chem Ecol 11:409–416

    Article  CAS  PubMed  Google Scholar 

  • Johnson LK, Hubbell SP (1974) Aggression and competition among stingless bees - field studies. Ecology 55(1):120–127

    Article  Google Scholar 

  • Johnson LK, Wiemer DF (1982) Nerol: an alarm substance of the stingless bee Trigona fulviventris (Hymenoptera: Apidae). J Chem Ecol 8(9):1167–1181

    Article  CAS  PubMed  Google Scholar 

  • 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 66:1–12

    Article  Google Scholar 

  • 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):761–766

    Article  CAS  PubMed  Google Scholar 

  • Kather R, Drijfhout FP, Martin SJ (2011) Task group differences in cuticular lipids in the honey bee Apis mellifera. J Chem Ecol 37:205–212

    Article  CAS  PubMed  Google Scholar 

  • Keller L, Nonacs P (1993) The role of queen pheromones in social insects: queen control or queen signal? Anim Behav 45:787–794

    Article  Google Scholar 

  • 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):611–618

    Article  Google Scholar 

  • Kerr WE, Zucchi R, Nakadaira JT, Botolo JD (1962) Reproduction in the social bees (Hymenoptera: Apidae). Journal of the New York Entomological Society 70:265–276

    Google Scholar 

  • Khoo SG, Yong HS (1987) Nest structure and colony defense in the stingless bee Trigona terminata Smith. Nature Malaysiana 12:4–15

    Google Scholar 

  • Kirchner WH, Friebe R (1999) Nestmate discrimination in the African stingless bee Hypotrigona gribodoi Magretti (Hymenoptera: Apidae). Apidologie 30(4):293–298

    Article  Google Scholar 

  • Langenheim JH (2003) Plant resins: chemistry, evolution, ecology and ethnobotany. Timber Press, Portland, p 586

    Google Scholar 

  • 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 47:17–21

    Article  Google Scholar 

  • 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 98:41–51

    Article  Google Scholar 

  • Leonhardt SD, Blüthgen N (2009a) A sticky affair: resin collection by Bornean stingless bees. Biotropica 41(6):730–736

    Article  Google Scholar 

  • Leonhardt SD, Blüthgen N, Schmitt T (2009b) Smelling like resin: terpenoids account for species-specific cuticular profiles in southeast-Asian stingless bees. Insect Soc 56:157–170

    Article  Google Scholar 

  • Leonhardt SD, Blüthgen N, Schmitt T (2010a) Chemical profiles of body surfaces and nests from six Bornean stingless bee species. J Chem Ecol 37:98–104

    Article  PubMed  CAS  Google Scholar 

  • Leonhardt SD, Jung L-M, Schmitt T, Blüthgen N (2010c) Terpenoids tame aggressors: role of chemicals in stingless bee communal nesting. Behav Ecol Sociobiol 64:1415–1423

    Article  Google Scholar 

  • Leonhardt SD, Menzel F, Nehring V, Schmitt T (2016) Ecology and evolution of communication in social insects. Cell 164(6):1277–1287

    Article  CAS  PubMed  Google Scholar 

  • 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):20130680

    Article  Google Scholar 

  • 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):e23445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leonhardt SD, Wallace HM, Blüthgen N, Wenzel F (2015) Potential role of environmentally derived cuticular compounds in stingless bees. Chemoecology (in press)

  • 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 36:537–543

    Article  Google Scholar 

  • Leonhardt SD, Zeilhofer S, Schmitt T (2010b) Stingless bees use terpenes as olfactory cues to find resin sources. Chem Senses 35:603–611

    Article  CAS  PubMed  Google Scholar 

  • Lichtenberg EM, Hrncir M, Turatti IC, Nieh JC (2011) Olfactory eavesdropping between two competing stingless bee species. Behav Ecol Sociobiol 65(4):763–774

    Article  PubMed  Google Scholar 

  • Lindauer M (1956) Über die Verständigung bei indischen Bienen. Z Vergl Phys 38:521–557

    Article  Google Scholar 

  • Lindauer M, Kerr WE (1958) Die gegenseitige Verständigung bei den stachellosen Bienen. Z Vergl Phys 41(4):405–434

    Article  Google Scholar 

  • Lindauer M, Kerr WE (1960) Communication between the workers of stingless bees. Bee World 41:29–41

    Article  Google Scholar 

  • 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 278:3593–3600

    Article  Google Scholar 

  • 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 19:1111–1127

    Article  CAS  Google Scholar 

  • 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 95:247–257

    Article  CAS  PubMed  Google Scholar 

  • 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 Res

  • Mc Cabe SI, Farina WM (2010) Olfactory learning in the stingless bee Tetragonisca angustula (Hymenoptera, Apidae, Meliponini). J Comp Physiol A 196(7):481–490

    Article  CAS  Google Scholar 

  • Michener CD (1974) The social behavior of the bees. Belknap Press of Harvard University Press, Cambridge, p 404

    Google Scholar 

  • Michener CD (1979) Biogeography of the bees. Ann Mo Bot Gard 66(3):277–347

    Article  Google Scholar 

  • Michener CD (2007) The bees of the world. John Hopkins University Press, Baltimore, London, p 953

    Google Scholar 

  • 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):432–439

    Article  PubMed  Google Scholar 

  • 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 38:1432–1440

    Article  CAS  PubMed  Google Scholar 

  • Nicolson SW (2011) Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two. Afr Zool 46(2):197–204

    Article  Google Scholar 

  • Nieh JC (2004) Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 35:159–182

    Article  Google Scholar 

  • 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)

  • 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 4:7449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 81:463–467

    Article  Google Scholar 

  • Nunes TM, Morgan ED, Drijfhout FP, Zucchi R (2010) Caste-specific cuticular lipids in the stingless bee Friesella schrottkyi. Apidologie 41:579–588

    Article  CAS  Google Scholar 

  • 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 75:1165–1171

    Article  Google Scholar 

  • 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):1172–1180

    Article  CAS  PubMed  Google Scholar 

  • 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):589–595

    Article  CAS  PubMed  Google Scholar 

  • Nunes TM, Von Zuben LG, Costa L, Venturieri GC (2014a) Defensive repertoire of the stingless bee Melipona flavolineata Friese (Hymenoptera: Apidae). Sociobiology 61(4):541–546

    Article  Google Scholar 

  • Paxton RJ, Weißschuh N, Engels W, Hartfelder K, Quezada-Euan JJG (1999) Not only single mating in stingless bees. Naturwissenschaften 86:143–146

    Article  CAS  Google Scholar 

  • 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 266:379–384

    Article  Google Scholar 

  • 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 40:331–340

    Article  CAS  PubMed  Google Scholar 

  • 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):817–823

    Article  Google Scholar 

  • Rasmussen C, Cameron SA (2010) Global stingless bee phylogeny supports ancient divergence, vicariance, and long distance dispersal. Biol J Linn Soc 99:206–232

    Article  Google Scholar 

  • Rebelo KS, Ferreira AG, Carvalho-Zilse GA (2016) Physicochemical characteristics of pollen collected by Amazonian stingless bees. Ciência Rural, Santa Maria 46(5):927–932

    Article  Google Scholar 

  • 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):243–249

    Article  CAS  Google Scholar 

  • 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):225–232

    Article  Google Scholar 

  • 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):519–524

    Article  CAS  PubMed  Google Scholar 

  • 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 14:495–501

    Article  CAS  PubMed  Google Scholar 

  • Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, New York, p 514

    Book  Google Scholar 

  • Roubik DW (2006) Stingless bee nesting biology. Apidologie 37(2):124–143

    Article  Google Scholar 

  • 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 61:1–10

    Article  PubMed  Google Scholar 

  • Roubik DW, Yanega D, Aluja M, Buchmann SL, Inouye DW (1995) On optimal nectar foraging by some tropical bees (Hymenoptera, Apidae). Apidologie 26:197–211

    Article  Google Scholar 

  • Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. Plant Syst Evol 222(1–4):187–209

    Article  CAS  Google Scholar 

  • 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 20:12525–12544

    Article  CAS  Google Scholar 

  • 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 19:507–511

    Article  CAS  Google Scholar 

  • 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):1153–1162

    Article  CAS  PubMed  Google Scholar 

  • 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 274:895–898

    Article  Google Scholar 

  • Schwarz HF (1948) Stingless bees of the western hemisphere. Bull Am Mus Nat Hist 90:1–546

    Google Scholar 

  • 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 37:72–80

    Article  CAS  Google Scholar 

  • 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):273–281

    Article  PubMed  Google Scholar 

  • 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):173–178

    Article  CAS  Google Scholar 

  • Simone M, Evans JD, Spivak M (2009) Resin collection and social immunity in honey bees. Evolution 63(11):3016–3022

    Article  CAS  PubMed  Google Scholar 

  • Simone-Finstrom M, Spivak M (2010) Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41(3):295–311

    Article  Google Scholar 

  • Simpson SJ, Raubenheimer D (2012) The nature of nutrition: a unifying framework from animal adaptation to human obesity. Princeton University Press, Princeton

    Book  Google Scholar 

  • 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 37:191–198

    Article  Google Scholar 

  • Slaa EJ, Tack AJM, Sommeijer MJ (2003) The effect of intrinsic and extrinsic factors on flower constancy in stingless bees. Apidologie 34:457–468

    Article  Google Scholar 

  • 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):1465–1472

    Article  CAS  PubMed  Google Scholar 

  • Sommeijer JM, De Bruijn LLM (1995) Drone congregations apart from the nest in Melipona favosa. Insect Soc 42:123–127

    Article  Google Scholar 

  • 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):38–44

    Article  Google Scholar 

  • Souza RCS, Yuyama LKO, Aguiar JPL, Oliveira FPM (2004) Valor nutricional do mel e pólen de abelhas sem ferrão da região amazônica. Acta Amazon 34:333–336

    Article  Google Scholar 

  • 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):13–19

    Article  CAS  Google Scholar 

  • Suka T, Inoue T (1993) Nestmate recognition of the stingless bee Trigona (Tetragonula) minangkabau (Apidae, Meliponinae). J Ethol 11(2):141–147

    Article  Google Scholar 

  • 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 338

    Google Scholar 

  • 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 17:376–383

    Article  CAS  PubMed  Google Scholar 

  • 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 343:287–290

    Article  CAS  PubMed  Google Scholar 

  • Van Veen WJ, Sommeijer JM (2000) Colony reproduction in Tetragonisca angustula (Apidae, Meliponini). Insect Soc 47(1):70–75

    Article  Google Scholar 

  • Van Veen JW, Sommeijer MJ, Meeuwsen JFJA (1997) Behaviour of drones in Melipona (Apidae, Meliponinae). Insect Soc 44:435–447

    Article  Google Scholar 

  • Vaudo AD, Tooker JF, Grozinger CM, Patch HM (2015) Bee nutrition and floral resource restoration. Current Opinion in Insect Science 10:133–141

    Article  Google Scholar 

  • 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):785–789

    CAS  PubMed  Google Scholar 

  • Velikova M, Bankova V, Tsvetkova I, Kujumgiev A, Marcucci MC (2000b) Antibacterial ent-kaurene from Brazilian propolis of native stingless bees. Fitoterapia 71(6):693–696

    Article  CAS  PubMed  Google Scholar 

  • 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):543–550

    Article  Google Scholar 

  • Vit P, Pedro SRM, Roubik D (2013) Pot-honey: a legacy of stingless bees. Springer, New York

    Book  Google Scholar 

  • Von Frisch K (1967) The dance language and orientation of bees. Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

  • Von Ihering H (1886) Der Stachel der Meliponen. Entomologische Nachrichten 12:177–188

    Google Scholar 

  • 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 63:339–347

    Article  Google Scholar 

  • 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):87–94

    Article  Google Scholar 

  • 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 41:428–435

    Article  Google Scholar 

  • Wallace HM, Trueman SJ (1995) Dispersal of Eucalyptus torelliana seeds by the resin-collecting stingless bee, Trigona carbonaria. Oecologia 104(1):12–16

    Article  CAS  PubMed  Google Scholar 

  • 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):479–494

    Article  CAS  Google Scholar 

  • Wille A (1983) Biology of the stingless bee. Annu Rev Entomol 28:41–46

    Article  Google Scholar 

  • Wilson EO (1971) The insect societies. Belknap Press of the Harvard University Press, pp 560

  • 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):e77512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):111–114

    Article  Google Scholar 

  • 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):631–641

    Article  CAS  PubMed  Google Scholar 

  • Zupko K, Sklan D, Lensky Y (1993) Proteins of the honeybee (Apis mellifera L.) body surface and exocrine gland secretions. J Insect Physiol 39:41–46

    Article  CAS  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sara Diana Leonhardt.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Leonhardt, S.D. Chemical Ecology of Stingless Bees. J Chem Ecol 43, 385–402 (2017). https://doi.org/10.1007/s10886-017-0837-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-017-0837-9

Keywords

Navigation