1932

Abstract

Stingless bees form perennial colonies of honey-making insects. The >600 species of stingless bees, mainly Neotropical, live throughout tropical latitudes. Foragers influence floral biology, plant reproduction, microbe dispersal, and diverse ecosystem functions. As tropical forest residents since the upper Cretaceous, they have had a long evolutionary history without competition from honey bees. Most stingless bees are smaller than any species and recruit nest mates to resources, while their defense strategies exclude stinging behavior but incorporate biting. Stingless bees have diversified ecologically; excel in nesting site selection and mutualisms with plants, arthropods, and microbes; and display opportunism, including co-opting plant defenses. As their biology becomes better known, applications to human endeavors are imposing selective pressures from exploitation and approaches to conservation that entail colony extraction from wildlands. Although some meliponines can adjust to new conditions, their populations shall require tropical diversity for survival and reproduction.

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2023-01-23
2024-04-27
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Literature Cited

  1. 1.
    Absy ML, Rech AR, Ferreira MG. 2018. Pollen collected by stingless bees: a contribution to understanding Amazonian biodiversity. See Reference 168 29–46
  2. 2.
    Al-Hatamleh MA, Boer JC, Wilson KL, Plebanski M, Mohamud R, Mustafa MZ 2020. Antioxidant-based medicinal properties of stingless bee products: recent progress and future directions. Biomolecules 10:923
    [Google Scholar]
  3. 3.
    Alvarez LJ, Reynaldi FJ, Ramello PJ, Garcia ML, Sguazza GH et al. 2018. Detection of honey bee viruses in Argentinian stingless bees (Hymenoptera: Apidae). Insect Soc. 65:191–97
    [Google Scholar]
  4. 4.
    Anholeti MC, de Pavia S, Figueiredo MRR, Kaplan MAC. 2015. Chemosystematic aspects of polisoprenylated benzophenones from the genus Clusia. Ann. Br. Acad. Sci. 87:289–01
    [Google Scholar]
  5. 5.
    Armbruster WS, Howard JJ, Clausen TP, Debevec EM, Loquvam JC et al. 1997. Do biochemical exaptations link evolution of plant defense and pollination systems? Historical hypotheses and experimental tests with Dalechampia vines. Am. Nat. 149:461–84
    [Google Scholar]
  6. 6.
    Arnold SEJ, Idrovo MEP, Arias LJL, Belmain SR, Stevenson PC. 2014. Herbivore defence compounds occur in pollen and reduce bumblebee colony fitness. J. Chem. Ecol. 40:878–81
    [Google Scholar]
  7. 7.
    Ávila S, Hornung PS, Teixeira GL, Malunga LN, Apea-Bah FB et al. 2019. Bioactive compounds and biological properties of Brazilian stingless bee honey have a strong relationship with the pollen floral origin. Food Res. Int. 123:1–10
    [Google Scholar]
  8. 8.
    Bänziger H. 2018. Congregations of tear drinking bees at human eyes: foraging strategies for an invaluable resource by Lisotrigona in Thailand (Apidae, Meliponini). Nat. Hist. Bull. Siam Soc. 62:161–93
    [Google Scholar]
  9. 9.
    Bänziger H, Bänziger S. 2010. Mammals, birds and reptiles as hosts of Lisotrigona bees, the tear drinkers with the broadest host range (Hymenoptera, Apidae). Mitt. Schweiz. Entomol. Gesellschaft. 83:271–82
    [Google Scholar]
  10. 10.
    Barbosa RN, Bezerra JD, Souza-Motta CM, Frisvad JC, Samson RA et al. 2018. New Penicillium and Talaromyces species from honey, pollen and nests of stingless bees. Antonie Van Leeuwenhoek 10:1883–12
    [Google Scholar]
  11. 11.
    Barth OM, Freitas AS, Almeida-Muradian LB, Vit P 2013. Palynological analysis of Brazilian stingless bee pot-honey. See Reference 169, ch. 4
  12. 12.
    Benton MJ, Wilf P, Sauquet H. 2022. The angiosperm revolution and the origins of modern biodiversity. New Phytol. 233:2017–35
    [Google Scholar]
  13. 13.
    Berenbaum MR, Calla R 2021. Honey as a functional food for Apis mellifera. . Annu. Rev. Entomol. 66:185–208
    [Google Scholar]
  14. 14.
    Bicalho B, Gonçalves RA, Zibordi AP, Manfio GP, Marsaioli AJ. 2003. Antimicrobial compounds of fungi vectored by Clusia spp. (Clusiaceae) pollinating bees. Z. Naturforsch. C 58:746–51
    [Google Scholar]
  15. 15.
    Brosi BJ. 2009. The complex responses of social stingless bees (Apidae: Meliponini) to tropical deforestation. Forest Ecol. Manag. 258:1830–37
    [Google Scholar]
  16. 16.
    Byrne DN, Hendrix DL, Williams LH III. 2003. Presence of trehalulose and other oligosaccharides in hemipteran honeydew, particularly Aleyrodidae. Physiol. Entomol. 28:144–49
    [Google Scholar]
  17. 17.
    Caesar L, Cibulski SP, Canal CW, Blochtein B, Sattler A, Haag KL. 2019. The virome of an endangered stingless bee suffering from annual mortality in southern Brazil. J. Gen. Virol. 100:1153–64
    [Google Scholar]
  18. 18.
    Camargo JMF. 2013. Historical biogeography of the Meliponini (Hymenoptera, Apidae, Apinae) of the Neotropical region. See Reference 168 19–34
    [Google Scholar]
  19. 19.
    Camargo JMF, Pedro SRM. 2004. Meliponini neotropicais: o gênero Ptilotrigona Moure (Hymenoptera, Apidae, Apinae). Rev. Bras. Entomol. 48:353–77
    [Google Scholar]
  20. 20.
    Camargo JMF, Pedro SRM 2007. Meliponini Lepeletier, 1836. Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region JS Moure, GAR Melo, D Urban 272–78 Curitiba, Bras.: Soc. Bras. Entomol.
    [Google Scholar]
  21. 21.
    Cameron EC, Franck P, Oldroyd BP. 2004. Genetic structure of nest aggregations and drone congregations of the southeast Asian stingless bee Trigona collina. . Mol. Ecol. 13:2357–64
    [Google Scholar]
  22. 22.
    Carvalho AF. 2022. Illegalities in the online trade of stingless bees in Brazil. Insect Conserv. Divers. In press
    [Google Scholar]
  23. 23.
    Cerqueira AMS, Hammer TJ, Moran NA, Santana WC, Kasuya MCM, da Silva CC. 2021. Extinction of anciently associated gut bacterial symbionts in a clade of stingless bees. ISME J. 15:2813–16
    [Google Scholar]
  24. 24.
    Chapman NC, Byatt M, Dos Santos Cocenza R, Nguyen NM, Heard TA et al. 2018. Anthropogenic hive movements are changing the genetic structure of a stingless bee Tetragonula carbonaria population along the east coast of Australia. Conserv. Gene 19:619–27
    [Google Scholar]
  25. 25.
    Chemurot M, Otim AS, Namayanja D, Onen H, Angiro C et al. 2021. Stingless beekeeping in Uganda: an industry in its infancy. Afr. Entomol. 29:165–72
    [Google Scholar]
  26. 26.
    Correia FD, Peruquetti RC, Ferreira MG, de Carvalho YK. 2016. Abundance and spatial distribution of nests of stingless bees (Apidae: Meliponini) and plant species used in the nesting in secondary forest fragment in Rio Branco-Acre. EntomoBrasilis 9:163–68
    [Google Scholar]
  27. 27.
    Cortopassi-Laurino M, Imperatriz-Fonseca VL, Roubik DW, Dollin A, Heard T et al. 2006. Global meliponiculture: challenges and opportunities. Apidologie 37:275–92
    [Google Scholar]
  28. 28.
    Cortopassi-Laurino M, Velthuis HHW, Nogueira-Neto P. 2007. Diversity of stingless bees from the Amazon forest of Xapuri (Acre), Brazil. Proc. Neth. Entomol. Soc. Meet. 18:105–14
    [Google Scholar]
  29. 29.
    da Silva Correia FC, Ferreira MG, Peruquetti RC, Gomes FA. 2020. Trophic resources collected by Melipona grandis Guérin, 1844 (Apidae: Meliponina) in rural area of Rio Branco, Acre-Brazil. Oecol. Aust. 24:676–87
    [Google Scholar]
  30. 30.
    Da-Costa T, dos Santos CF, Rodighero LF, Ferla NJ, Blochtein B. 2021. Mite diversity is determined by the stingless bee host species. Apidologie 52:950–59
    [Google Scholar]
  31. 31.
    Dario MA, Lisboa CV, Silva MV, Herrera HM, Rocha FL et al. 2021. Crithidia mellificae infection in different mammalian species in Brazil. Int. J. Parasitol. Parasites Wildl. 15:58–59
    [Google Scholar]
  32. 32.
    de Novais JS, Garcêz AC, Absy ML, Francisco de Assis R. 2015. Comparative pollen spectra of Tetragonisca angustula (Apidae, Meliponini) from the Lower Amazon (N Brazil) and caatinga (NE Brazil). Apidologie 46:417–31
    [Google Scholar]
  33. 33.
    de Paula GT, Menezes C, Pupo MT, Rosa CA. 2021. Stingless bees and microbial interactions. Curr. Opin. Insect Sci. 44:41–47
    [Google Scholar]
  34. 34.
    de Sousa LP. 2021. Bacterial communities of indoor surface of stingless bee nests. PLOS ONE 16:7e0252933
    [Google Scholar]
  35. 35.
    de Souza FS, Kevill JL, Correia-Oliveira ME, de Carvalho CA, Martin SJ. 2019. Occurrence of deformed wing virus variants in the stingless bee Melipona subnitida and honey bee Apis mellifera populations in Brazil. J. Gen. Virol. 100:289–94
    [Google Scholar]
  36. 36.
    de Souza RR, de Abreu VH, de Novais JS. 2019. Melissopalynology in Brazil: a map of pollen types and published productions between 2005 and 2017. Palynology 43:690–700
    [Google Scholar]
  37. 37.
    Del-Claro K, Lange D, Torezan-Silingardi HM, Anjo DV, Calixto ES et al. 2018. The complex ant-plant relationship within tropical ecological networks. Ecological Networks in the Tropics W Dáttilo, V Rico-Gray 59–71 Berlin: Springer
    [Google Scholar]
  38. 38.
    Delgado C, Mejía K, Rasmussen C. 2020. Management practices and honey characteristics of Melipona eburnea in the Peruvian Amazon. Ciênc. Rural 23:50
    [Google Scholar]
  39. 39.
    Dharampal PS, Carlson C, Currie CR, Steffan SA. 2019. Pollen-borne microbes shape bee fitness. Proc. R. Soc. B 286:20182894
    [Google Scholar]
  40. 40.
    Díaz S, de Souza Urbano S, Caesar L, Blochtein B, Sattler A et al. 2017. Report on the microbiota of Melipona quadrifasciata affected by a recurrent disease. J. Invertebr. Pathol. 143:35–39
    [Google Scholar]
  41. 41.
    Domingos SC, Clebis VH, Nakazato G, de Oliveira AG Jr., Takayama Kobayashi RK et al. 2021. Antibacterial activity of honeys from Amazonian stingless bees of Melipona spp. and its effects on bacterial cell morphology. J. Sci. Food Agric. 101:2072–77
    [Google Scholar]
  42. 42.
    Dorian NN, Bonoan RE. 2016. Salt foraging of stingless bees at La Selva Biological Station, Costa Rica. Bee World 93:61–63
    [Google Scholar]
  43. 43.
    dos Santos CF, Acosta AL, Halinski R, de Souza dos Santos PD, Borges RC et al. 2022. The widespread trade in stingless beehives may introduce them into novel places and could threaten species. J. Appl. Ecol. 59:965–81
    [Google Scholar]
  44. 44.
    dos Santos CF, Halinski R, de Souza dos Santos PD, Almeida EA, Blochtein B. 2019. Looking beyond the flowers: associations of stingless bees with sap-sucking insects. Sci. Nat. 106:12
    [Google Scholar]
  45. 45.
    Draper FC, Costa FR, Arellano G, Phillips OL, Duque A et al. 2020. Amazon tree dominance across forest strata. Nat. Ecol. Evol. 5:757–67
    [Google Scholar]
  46. 46.
    Drescher N, Wallace HM, Katouli M, Massaro CF, Leonhardt SD. 2014. Diversity matters: how bees benefit from different resin sources. Oecologia 176:943–53
    [Google Scholar]
  47. 47.
    Eckles MA, Roubik DW, Nieh JC. 2012. A stingless bee can use visual odometry to estimate both height and distance. J. Exp. Biol. 215:3155–60
    [Google Scholar]
  48. 48.
    Elias-Santos D, Maria do Carmo QF, Vitorino R, Oliveira LL, Zanuncio JC, Serrão JE 2013. Proteome of the head and thorax salivary glands in the stingless bee Melipona quadrifasciata anthidioides. Apidologie 44:684–98
    [Google Scholar]
  49. 49.
    Eltz T, Brühl CA, Görke C. 2002. Collection of mold (Rhizopus sp.) spores in lieu of pollen by the stingless bee Trigona collina. Insect. Soc. 49:28–30
    [Google Scholar]
  50. 50.
    Eltz T, Brühl CA, Imiyabir Z, Linsenmair KE. 2003. Nesting and nest trees of stingless bees (Apidae: Meliponini) in lowland dipterocarp forests in Sabah, Malaysia, with implications for forest management. For. Ecol. Manag. 172:301–13
    [Google Scholar]
  51. 51.
    Engel MS, Herhold H, Davis S, Wang B, Thomas J 2021. Stingless bees in Miocene amber of southeastern China (Hymenoptera: Apidae). J. Melittol. 105:1–88
    [Google Scholar]
  52. 52.
    Figueroa LL, Blinder M, Grincavitch C, Jelinek A, Mann EK et al. 2019. Bee pathogen transmission dynamics: deposition, persistence and acquisition on flowers. Proc. R. Soc. B 286:20190603
    [Google Scholar]
  53. 53.
    Figueroa LL, Maccaro JJ, Krichilsky E, Yanega D, McFrederick QS. 2021. Why did the bee eat the chicken? Symbiont gain, loss, and retention in the vulture bee microbiome. mBio 12:e02317–21
    [Google Scholar]
  54. 54.
    Fletcher MT, Hungerford NL, Webber D, de Jesus MC, Zhang J et al. 2020. Stingless bee honey, a novel source of trehalulose: a biologically active disaccharide with health benefits. Sci. Rep. 10:12128
    [Google Scholar]
  55. 55.
    Gilliam M, Buchmann SL, Lorenz BJ, Roubik DW. 1985. Microbiology of the larval provisions of the stingless bee, Trigona hypogea, an obligate necrophage. Biotropica 17:28–31
    [Google Scholar]
  56. 56.
    Gilliam M, Roubik DW, Lorenz BJ. 1990. Microorganisms associated with pollen, honey, and brood provisions in the nest of a stingless bee, Melipona fasciata. Apidologie 21:89–97
    [Google Scholar]
  57. 57.
    Gonçalves P, Gonçalves C, Brito PH, Sampaio JP. 2020. The Wickerhamiella/Starmerella clade—a treasure trove for the study of the evolution of yeast metabolism. Yeast 37:313–20
    [Google Scholar]
  58. 58.
    Grüter C. 2020. Stingless Bees Berlin: Springer
  59. 59.
    Grüter C, Segers FH, Menezes C, Vollet-Neto A, Falcón T et al. 2017. Repeated evolution of soldier sub-castes suggests parasitism drives social complexity in stingless bees. Nat. Commun. 8:4
    [Google Scholar]
  60. 60.
    Guimarães-Cestaro L, Martins MF, Martínez LC, Alves ML, Guidugli-Lazzarini KR et al. 2020. Occurrence of virus, microsporidia, and pesticide residues in three species of stingless bees (Apidae: Meliponini) in the field. Sci. Nat. 107:16
    [Google Scholar]
  61. 61.
    Guzmán-Novoa E, Hamiduzzaman MM, Anguiano-Baez R, Correa-Benítez A, Castañeda-Cervantes E, Arnold NI. 2015. First detection of honey bee viruses in stingless bees in North America. J. Apic. Res. 54:93–95
    [Google Scholar]
  62. 62.
    Hall MA, Brettell LE, Liu H, Nacko S, Spooner-Hart R et al. 2020. Temporal changes in the microbiome of stingless bee foragers following colony relocation. FEMS Microbiol. Ecol. 97:fiaa236
    [Google Scholar]
  63. 63.
    Heard TA. 2016. The Australian Native Bee Book: Keeping Stingless Bee Hives for Pets, Pollination and Sugarbag Honey. Brisbane, Aust.: Sugarbag Bees
  64. 64.
    Hilgert-Moreira SB, Nascher CA, Callegari-Jacques SM, Blochtein B. 2014. Pollen resources and trophic niche breadth of Apis mellifera and Melipona obscurior (Hymenoptera, Apidae) in a subtropical climate in the Atlantic rain forest of southern Brazil. Apidologie 45:129–41
    [Google Scholar]
  65. 65.
    Hrncir M, Maia-Silva C, da Silva Teixeira-Souza VH, Imperatriz-Fonseca VL. 2019. Stingless bees and their adaptations to extreme environments. J. Comp. Physiol. A 205:415–26
    [Google Scholar]
  66. 66.
    Hubbell SP, Johnson LK. 1977. Competition and nest spacing in a tropical stingless bee community. Ecology 58:949–63
    [Google Scholar]
  67. 67.
    Imbach P, Fung E, Hannah L, Navarro-Racines CE, Roubik DW et al. 2017. Coffee, bees and climate: coupling of pollination services and agriculture under climate change. PNAS 114:10438–42
    [Google Scholar]
  68. 68.
    Janzen DH. 1975. Ecology of Plants in the Tropics London: Edward Arnold
  69. 69.
    Jaffé R, Pope N, Carvalho NT, Maia UM, Blochtein B et al. 2018. Bees for development: Brazilian survey reveals how to optimize stingless beekeeping. PLOS ONE 9:e105718
    [Google Scholar]
  70. 70.
    Kajobe R, Roubik DW. 2006. Honey-making bee colony abundance and predation by apes and humans in a Uganda forest reserve. Biotropica 38:210–18
    [Google Scholar]
  71. 71.
    Kaluza BF, Wallace HM, Heard TA, Minden V, Klein A, Leonhardt SD. 2018. Social bees are fitter in more biodiverse environments. Sci. Rep. 8:12353
    [Google Scholar]
  72. 72.
    Kämper W, Kaluza BF, Wallace H, Schmitt T, Leonhardt SD. 2019. Habitats shape the cuticular chemical profiles of stingless bees. Chemoecology 29:125–33
    [Google Scholar]
  73. 73.
    Kiatoko N, Raina SK, van Langevelde F. 2017. Impact of habitat degradation on species diversity and nest abundance of five African stingless bee species in a tropical rainforest of Kenya. Int. J. Trop. Insect Sci. 37:189–97
    [Google Scholar]
  74. 74.
    Koch H, Abrol DP, Li J, Schmid-Hempel P. 2013. Diversity and evolutionary patterns of bacterial gut associates of corbiculate bees. Mol. Ecol. 22:2028–44
    [Google Scholar]
  75. 75.
    Koch H, Corcoran C, Jonker M. 2011. Honeydew collecting in Malagasy stingless bees (Hymenoptera: Apidae: Meliponini) and observations on competition with invasive ants. Afr. Entomol. 19:36–41
    [Google Scholar]
  76. 76.
    Koethe S, Fischbach V, Banysch S, Reinartz L, Hrncir M, Lunau K. 2020. A comparative study of food source selection in stingless bees and honeybees: scent marks, location, or color. Front. Plant Sci. 11:516
    [Google Scholar]
  77. 77.
    Kondo T, Roubik DW. 2022. Description of a new ant- and stingless-bee-loving species of Cryptostigma Ferris (Hemiptera: Coccomorpha: Coccidae) from Ecuador living inside internodes of Cecropia (Urticaceae), with an updated key to the adult females and first-instar nymphs of the genus. Zootaxa 5190:454354
    [Google Scholar]
  78. 78.
    Kwong WK, Medina LA, Koch H, Sing KW, Soh EJ et al. 2017. Dynamic microbiome evolution in social bees. Sci. Adv. 3:e1600513
    [Google Scholar]
  79. 79.
    Leonhardt SD. 2017. Chemical ecology of stingless bees. J. Chem. Ecol. 43:385–402
    [Google Scholar]
  80. 80.
    Leonhardt SD, Baumann AM, Wallace HM, Brooks P, Schmitt T. 2014. The chemistry of an unusual seed dispersal mutualism: Bees use a complex set of olfactory cues to find their partner. Anim. Behav. 98:41–51
    [Google Scholar]
  81. 81.
    Leonhardt SD, Kaltenpoth M. 2014. Microbial communities of three sympatric Australian stingless bee species. PLOS ONE 9:e105718
    [Google Scholar]
  82. 82.
    Leonhardt SD, Rasmussen C, Schmitt T. 2013. Genes versus environment: Geography and phylogenetic relationships shape the chemical profiles of stingless bees on a global scale. Proc. R. Soc. B 280:20130680
    [Google Scholar]
  83. 83.
    Lorenzon MCA, Matrangolo CAR. 2005. Foraging on some nonfloral resources by stingless bees (Hymenoptera, Meliponini) in a Caatinga region. Braz. J. Biol. 65:291–98
    [Google Scholar]
  84. 84.
    Marín-Henao D, Quijano-Abril M, Giraldo Sánchez CE, Calvo-Cardona SJ, Zapata-Vahos IC 2022. Limited foraging overlap between introduced Apis mellifera and native Melipona eburnea in a Colombian moist forest as revealed through pollen analysis. Palynology 46:1–14
    [Google Scholar]
  85. 85.
    Marques-Souza AC, Absy ML, Kerr WE. 2007. Pollen harvest features of the Central Amazonian bee Scaptotrigona fulvicutis Moure 1964 (Apidae: Meliponinae), in Brazil. Acta Bot. Bras. 21:11–20
    [Google Scholar]
  86. 86.
    Martins AC, Melo GA, Renner SS. 2014. The corbiculate bees arose from New World oil-collecting bees: implications for the origin of pollen baskets. Mol. Phylogenet. Evol. 80:88–94
    [Google Scholar]
  87. 87.
    Mateus S, Noll FB. 2004. Predatory behavior in a necrophagous bee Trigona hypogea (Hymenoptera; Apidae, Meliponini). Naturwissenschaften 91:94–96
    [Google Scholar]
  88. 88.
    McFrederick QS, Wcislo WT, Taylor DR, Ishak HD, Dowd SE, Mueller UG. 2012. Environment or kin: Whence do bees obtain acidophilic bacteria?. Mol. Ecol. 21:1754–68
    [Google Scholar]
  89. 89.
    McMahon DP, Fürst MA, Caspar J, Theodorou P, Brown MJ, Paxton RJ. 2015. A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees. J. Anim. Ecol. 84:615–24
    [Google Scholar]
  90. 90.
    Medina-Franco J. 2020. Towards a unified Latin American natural products database: LANaPD. Future Sci. OA 6:FSO468
    [Google Scholar]
  91. 91.
    Menegatti C, Fukuda TT, Pupo MT. 2021. Chemical ecology in insect-microbe interactions in the neotropics. Planta Med. 87:38–48
    [Google Scholar]
  92. 92.
    Menegatti C, Lourenzon VB, Rodríguez-Hernández D, Melo GDP, Ferreira LLG et al. 2020. Meliponamycins: antimicrobials from stingless bee-associated Streptomyces sp. . J. Nat. Prod. 83:610–16
    [Google Scholar]
  93. 93.
    Michener CD. 1979. Biogeography of the bees. Ann. Mo. Bot. Gard. 1:277–347
    [Google Scholar]
  94. 94.
    Michener CD. 2007. The Bees of the World Baltimore, MD: Johns Hopkins Univ. Press. , 2nd ed..
  95. 95.
    Mirhosseini H, Amid BT. 2012. A review study on chemical composition and molecular structure of newly plant gum exudates and seed gums. Food Res. Int. 46:387–98
    [Google Scholar]
  96. 96.
    Mohammad SM, Mahmud-Ab-Rashid NK, Zawawi N 2021. Stingless bee-collected pollen (bee bread): chemical and microbiology properties and health benefits. Molecules 26:957
    [Google Scholar]
  97. 97.
    Ng WJ, Sit NW, Ooi PA, Ee KY, Lim TM. 2020. The antibacterial potential of honeydew honey produced by stingless bee (Heterotrigona itama) against antibiotic resistant bacteria. Antibiotics 9:871
    [Google Scholar]
  98. 98.
    Nieh JC, Barreto LS, Contrera FA, Imperatriz-Fonseca VL. 2004. Olfactory eavesdropping by a competitively foraging stingless bee, Trigona spinipes. Proc. R. Soc. Lond. B 271:15481633–40
    [Google Scholar]
  99. 99.
    Nieh JC, Roubik DW. 1995. A stingless bee (Melipona panamica) indicates food location without using a scent trail. Behav. Ecol. Sociobiol. 37:63–70
    [Google Scholar]
  100. 100.
    Njau MA, Mturi FA, Mpuya PM. 2010. Options for stingless honey-beekeeping around Udzungwa Mountains National Park, Tanzania, and implications for biodiversity management. Int. J. Biodivers. Sci. Ecosyst. Serv. Manag. 6:89–95
    [Google Scholar]
  101. 101.
    Noll FB, Zucchi R, Jorge JA, Mateus S 1996. Food collection and maturation in the necrophagous stingless bee, Trigona hypogea (Hymenoptera: Meliponinae). J. Kans. Entomol. Soc. 69:287–93
    [Google Scholar]
  102. 102.
    Nunes TM, Turatti IC, Lopes NP, Zucchi R. 2009. Chemical signals in the stingless bee, Frieseomelitta varia, indicate caste, gender, age, and reproductive status. J. Chem. Ecol. 35:1172–80
    [Google Scholar]
  103. 103.
    Nunes-Silva P, Costa L, Campbell AJ, Arruda H, Contrera FA et al. 2020. Radiofrequency identification (RFID) reveals long-distance flight and homing abilities of the stingless bee Melipona fasciculata. Apidologie 51:240–53
    [Google Scholar]
  104. 104.
    Oliveira DD, de Carvalho CA, Sodré GD, Paixão JF, Alves RM. 2017. Partitioning of pollen resources by two stingless bee species in the north Bahia, Brazil. Grana 56:285–93
    [Google Scholar]
  105. 105.
    Oliveira DD, Rodrigues dos Santos D, Andrade BR, Nascimento AS, Oliveira da Silva M et al. 2021. Botanical origin, microbiological quality and physicochemical composition of the Melipona scutellaris pot-pollen (“samburá”) from Bahia (Brazil) Region. J. Apic. Res. 60:457–69
    [Google Scholar]
  106. 106.
    Oliveira ML, Morato EF. 2000. Stingless bees (Hymenoptera, Meliponini) feeding on stinkhorn spores (Fungi, Phallales): robbery or dispersal?. Rev. Bras. Zool. 17:881–84
    [Google Scholar]
  107. 107.
    Orr MC, Hughes AC, Chesters D, Pickering J, Zhu CD, Ascher JS. 2021. Global patterns and drivers of bee distribution. Curr. Biol. 31:451–58
    [Google Scholar]
  108. 108.
    Palmer-Young EC, Farrell IW, Adler LS, Milano NJ, Egan PA et al. 2019. Chemistry of floral rewards: intra- and interspecific variability of nectar and pollen secondary metabolites across taxa. Ecol. Monogr. 89:e01335
    [Google Scholar]
  109. 109.
    Paludo CR, Menezes C, Silva EA, Vollet-Neto A, Andrade-Dominguez A et al. 2018. Stingless bee larvae require fungal steroid to pupate. Sci. Rep. 8:1122
    [Google Scholar]
  110. 110.
    Pedro SRM. 2014. The stingless bee fauna in Brazil (Hymenoptera: Apidae). Sociobiology 61:348–54
    [Google Scholar]
  111. 111.
    Pérez-Pérez EM, Suárez E, Peña-Vera MJ, González AC, Vit P. 2013. Antioxidant activity and microorganisms in nest products of Tetragonisca angustula Latreille, 1811 from Mérida, Venezuela. See Reference 169, ch. 10
  112. 112.
    Peronti ALBG, Fernandes LBR, Fernandes MA. 2013. A facultative association between Plebeia droryana (Friese, 1900) (Hymenoptera: Apidae: Meliponini) and a wax scale insect, Ceroplastes janeirensis (Hemiptera: Cocoidea: Cocidae). Braz. J. Biol. 73:453–54
    [Google Scholar]
  113. 113.
    Peng T, Schroeder M, Grüter C. 2020. Octopamine increases individual and collective foraging in a neotropical stingless bee. Biol. Lett. 16:620200238
    [Google Scholar]
  114. 114.
    Popova M, Gerginova D, Trusheva B, Simova S, Tamfu AN et al. 2021. A preliminary study of chemical profiles of honey, cerumen, and propolis of the African stingless bee Meliponula ferruginea. . Foods 10:997
    [Google Scholar]
  115. 115.
    Popova M, Trusheva B, Bankova V. 2021. Propolis of stingless bees: a phytochemist's guide through the jungle of tropical biodiversity. Phytomedicine 86:153098
    [Google Scholar]
  116. 116.
    Posey DA, Camargo JMF. 1985. Additional notes on beekeeping of Meliponinae by the Kayapó Indians of Brazil. Ann. Carnegie Mus. Nat. Hist. 54:247–74
    [Google Scholar]
  117. 117.
    Price RA, Segers F, Berger A, Nascimento FS, Grüter C. 2021. An exploration of the relationship between recruitment communication and foraging in stingless bees. Curr. Zool. 67:551–60
    [Google Scholar]
  118. 118.
    Purkiss T, Lach L. 2019. Pathogen spillover from Apis mellifera to a stingless bee. Proc. R. Soc. B 286:20191071
    [Google Scholar]
  119. 119.
    Quezada-Euán JJG, Nates-Parra G, Maués MM, Imperatriz-Fonseca VL, Roubik DW 2018. The economic and cultural values of stingless bees (Hymenoptera: Meliponini) among ethnic groups of tropical America. Sociobiology 65:534–57
    [Google Scholar]
  120. 120.
    Ramalho M, Giannini TC, Malagodi-Braga KS, Imperatriz-Fonseca VL. 1994. Pollen harvest by stingless bee foragers (Hymenoptera, Apidae, Meliponinae). Grana 33:239–44
    [Google Scholar]
  121. 121.
    Ramalho M, Kleinert-Giovannini A, Imperatriz-Fonseca VL. 1990. Important bee plants of stingless bees (Melipona and Trigonini) and Africanized honeybees (Apis mellifera) in neotropical habitats: a review. Apidologie 21:469–88
    [Google Scholar]
  122. 122.
    Ramalho M, Silva MD, Carvalho CA. 2007. Harvesting dynamics of pollen sources by Melipona scutellaris Latreille (Hymenoptera: Apidae): a comparative analysis with Apis mellifera L. (Hymenoptera: Apidae) in the Atlantic Forest Domain. Neotrop. Entomol. 36:38–45
    [Google Scholar]
  123. 123.
    Ramirez SR, Nieh JC, Quental TB, Roubik DW, Imperatriz-Fonseca VL, Pierce NI 2010. Molecular phylogeny of the stingless bee genus Melipona (Hymenoptera: Apidae) and the evolution of recruitment communication in eusocial Apidae. Mol. Phylogenet. Evol. 56:519–25
    [Google Scholar]
  124. 124.
    Rasmussen C, Camargo JMF. 2008. A molecular phylogeny and the evolution of nest architecture and behavior in Trigona s. s. (Hymenoptera: Apidae, Meliponini). Apidologie 39:102–18
    [Google Scholar]
  125. 125.
    Rasmussen C, Cameron S 2010. Global stingless bee phylogeny supports ancient divergence, vicariance, and long distance dispersal. Biol. J. Linn. Soc. 99:206–32
    [Google Scholar]
  126. 126.
    Rego JO, Oliveira R, Jacobi CM, Schlindwein C. 2018. Constant flower damage caused by a common stingless bee puts survival of a threatened buzz-pollinated species at risk. Apidologie 49:276–86
    [Google Scholar]
  127. 127.
    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 197:243–49
    [Google Scholar]
  128. 128.
    Rezende ACC, Absy ML, Ferreira MG. 2020. Pollen niche of Melipona dubia, Melipona seminigra and Scaptotrigona sp. (Apidae: Meliponini) kept in indigenous communities of the Sateré Mawé Tribe, Amazonas, Brazil. J. Apic. Res. 12: https://doi.org/10.1080/00218839.2020.1861755
    [Crossref] [Google Scholar]
  129. 129.
    Rivest S, Forrest JR. 2020. Defence compounds in pollen: Why do they occur and how do they affect the ecology and evolution of bees?. New Phytol. 225:1053–64
    [Google Scholar]
  130. 130.
    Rodrígues CS, Ferasso DC, Mosse AJ, Coelho GC. 2020. Pollen resources partitioning of stingless bees (Hymenoptera: Apidae) from the southern Atlantic Forest. Acta Sci. 42:1–9
    [Google Scholar]
  131. 131.
    Rosli FN, Hazemi MH, Akbar MA, Basir S, Kassim H, Bunawan H. 2020. Stingless bee honey: evaluating its antibacterial activity and bacterial diversity. Insects 11:500
    [Google Scholar]
  132. 132.
    Roubik DW. 1982. Obligate necrophagy in a social bee. Science 217:1059–60
    [Google Scholar]
  133. 133.
    Roubik DW. 1989. Ecology and Natural History of Tropical Bees Cambridge, UK: Cambridge Univ. Press
  134. 134.
    Roubik DW 1990. Niche preemption in tropical bee communities: a comparison of Neotropical and Malesian faunas. Natural History of Social Wasps and Bees in Equatorial Sumatra SF Sakagami, R Ohgushi, DW Roubik 245–57 Sapporo, Jpn: Hokkaido Univ.
    [Google Scholar]
  135. 135.
    Roubik DW 1992. Loose niches in tropical communities: Why are there so few bees and so many trees?. Effects of Resource Distribution on Plant-Animal Interactions M Hunter, T Ohgushi, PW Price 327–54 New York: Academic
    [Google Scholar]
  136. 136.
    Roubik DW. 1993. Direct costs of forest reproduction, bee-cycling and the efficiency of pollination modes. J. Biosci. 18:537–52
    [Google Scholar]
  137. 137.
    Roubik DW 1996. African honey bees as exotic pollinators in French Guiana. The Conservation of Bees A Matheson, SL Buchmann, C O'Toole, P Westrich, IH Williams 173–82 New York: Academic
    [Google Scholar]
  138. 138.
    Roubik DW 1996. Order and chaos in tropical bee communities. Anais do II Encontro Sobre Abelhas de Ribeirão Preto CA Garofalo et al.122–32 São Paulo: Univ. São Paulo
    [Google Scholar]
  139. 139.
    Roubik DW. 2006. Stingless bee nesting biology. Apidologie 37:124–43
    [Google Scholar]
  140. 140.
    Roubik DW. 2018. 100 species of meliponines (Apidae: Meliponini) in a parcel of western Amazonian forest at Yasuní Biosphere Reserve, Ecuador. See Reference 168 189–206
    [Google Scholar]
  141. 141.
    Roubik DW. 2021. Mutualism within a parasitism within a mutualism: the bees and coccids that inhabit Cecropia ant-plants. Ecology 102:e03367
    [Google Scholar]
  142. 142.
    Roubik DW 2023. Working with Neotropical Trigona on Barro Colorado Island (Apinae: Meliponini). 100 Years of Studies on Barro Colorado Island SJ Wright et al. Washington, DC: Smithsonian. In press
    [Google Scholar]
  143. 143.
    Roubik DW, Moreno Patiño JE. 2009. Trigona corvina: an ecological study based on unusual nest structure and pollen analysis. Psyche 2009:268756
    [Google Scholar]
  144. 144.
    Roubik DW, Moreno Patiño JE. 2013. How to be a bee-botanist using pollen spectra. See Reference 167 295–314
    [Google Scholar]
  145. 145.
    Roubik DW, Moreno Patiño JE. 2018. The stingless honey bees (Apidae, Apinae: Meliponini) in Panama and pollination ecology from pollen analysis. See Reference 168 47–66
  146. 146.
    Roubik DW, Vergara CA 2021. Geographic distribution of bees: a history and an update. Good Bee Keeping Practices for Sustainable Apiculture G Formato 11–14 Rome: Food Agric. Organ. U. N.
    [Google Scholar]
  147. 147.
    Roumy V, Fabre N, Portet B, Bourdy G, Acebey L et al. 2009. Four anti-protozoal and anti-bacterial compounds from Tapirira guianensis. Phytochemistry 70:305–11
    [Google Scholar]
  148. 148.
    Schorkopf DL. 2016. Male meliponine bees (Scaptotrigona aff. depilis) produce alarm pheromones to which workers respond with fight and males with flight. J. Comp. Physiol. A 202:667–78
    [Google Scholar]
  149. 149.
    Seeley TD. 1985. Honeybee Ecology: A Study of Adaptation in Social Life Princeton, NJ: Princeton Univ. Press
  150. 150.
    Shanahan M, Spivak M. 2021. Resin use by stingless bees: a review. Insects 12:719
    [Google Scholar]
  151. 151.
    Silva TM, Camara CA, da Silva Lins AC, Barbosa-Filho JM, da Silva EM et al. 2006. Chemical composition and free radical scavenging activity of pollen loads from stingless bee Melipona subnitida Ducke. J. Food Compos. Anal. 19:507–11
    [Google Scholar]
  152. 152.
    Slaa EJ, Chaves LAS, Malagodi-Braga KS, Hofstede FE. 2006. Stingless bees in applied pollination: practice and perspectives. Apidologie 37:293–315
    [Google Scholar]
  153. 153.
    Souza ECA, Menezes C, Flach A. 2021. Stingless bee honey (Hymenoptera, Apidae, Meliponini): a review of quality control, chemical profile, and biological potential. Apidologie 52:113–32
    [Google Scholar]
  154. 154.
    Souza-Junior JB, da Silva Teixeira-Souza VH, Oliveira-Souza A, de Oliveira PF, de Queiroz JP, Hrncir M. 2020. Increasing thermal stress with flight distance in stingless bees (Melipona subnitida) in the Brazilian tropical dry forest: implications for constraint on foraging range. J. Insect Physiol. 123:104056
    [Google Scholar]
  155. 155.
    Stearman AM, Stierlin E, Sigman ME, Roubik DW, Dorrien D. 2008. Stradivarius in the jungle: traditional knowledge and the use of “black beeswax” among the Yuquí of the Bolivian Amazon. Hum. Ecol. 36:149–59
    [Google Scholar]
  156. 156.
    Steffan SA, Dharampal PS, Danforth BN, Gaines-Day HR, Takizawa Y, Chikaraishi Y. 2019. Omnivory in bees: elevated trophic positions among all major bee families. Am. Nat. 194:414–21
    [Google Scholar]
  157. 157.
    Streinzer M, Huber W, Spaethe J. 2016. Body size limits dim-light foraging activity in stingless bees (Apidae: Meliponini). J. Comp. Physiol. A 202:643–55
    [Google Scholar]
  158. 158.
    Tamarit D, Ellegaard KM, Wikander J, Olofsson T, Vasquez A, Andersson SG. 2015. Functionally structured genomes in Lactobacillus kunkeei colonizing the honey crop and food products of honeybees and stingless bees. Genome Biol. Evol. 7:1455–73
    [Google Scholar]
  159. 159.
    Tang QH, Miao CH, Chen YF, Dong ZX, Cao Z et al. 2021. The composition of bacteria in gut and beebread of stingless bees (Apidae: Meliponini) from tropics Yunnan, China. Antonie Van Leeuwenhoek 114:1293–305
    [Google Scholar]
  160. 160.
    Tola YH, Waweru JW, Ndungu NN, Nkoba K, Slippers B, Paredes JC. 2021. Loss and gain of gut bacterial phylotype symbionts in Afrotropical stingless bee species (Apidae: Meliponinae). Microorganisms 9:2420
    [Google Scholar]
  161. 161.
    Tölke ED, Demarco D, Carmello-Guerreiro SM, Bachelier JB 2021. Flower structure and development of Spondias tuberosa and Tapirira guianensis (Spondioideae): implications for the evolution of the unisexual flowers and pseudomonomery in Anacardiaceae. Int. J. Plant Sci. 182:747–62
    [Google Scholar]
  162. 162.
    Tran TD, Ogbourne SM, Brooks PR, Sánchez-Cruz N, Medina-Franco JL, Quinn RJ. 2020. Lessons from exploring chemical space and chemical diversity of propolis components. Int. J. Mol. Sci. 21:4988
    [Google Scholar]
  163. 163.
    Trinkl M, Kaluza BF, Wallace H, Heard TA, Keller A, Leonhardt SD. 2020. Floral species richness correlates with changes in the nutritional quality of larval diets in a stingless bee. Insects 11:125
    [Google Scholar]
  164. 164.
    Van Oystaeyen A, Alves DA, Oliveira RC, do Nascimento DL, do Nascimento FS et al. 2013. Sneaky queens in Melipona bees selectively detect and infiltrate queenless colonies. Anim. Behav. 86:603–9
    [Google Scholar]
  165. 165.
    Vannette RL. 2020. The floral microbiome: plant, pollinator, and microbial perspectives. Annu. Rev. Ecol. Evol. Syst. 51:363–86
    [Google Scholar]
  166. 166.
    Villacrés-Granda I, Coello D, Proaño A, Ballesteros I, Roubik DW et al. 2021. Honey quality parameters, chemical composition and antimicrobial activity in twelve Ecuadorian stingless bees (Apidae: Apinae: Meliponini) tested against multiresistant human pathogens. LWT 140:110737
    [Google Scholar]
  167. 167.
    Vit P, Pedro SRM, Roubik DW, eds. 2013. Pot-Honey: A Legacy of Stingless Bees Berlin: Springer
  168. 168.
    Vit P, Pedro SRM, Roubik DW, eds. 2018. Pot-Pollen in Stingless Bee Melittology Berlin: Springer
  169. 169.
    Vit P, Roubik DW, eds. 2013.. Stingless Bees Process Honey and Pollen in Cerumen Pots Mérida, Venez.: Univ. Los Andes http://www.saber.ula.ve/handle/123456789/35292
  170. 170.
    Vollet-Neto A, Koffler S, dos Santos CF, Menezes C, Nunes FMF et al. 2018. Recent advances in reproductive biology of stingless bees. Insect. Soc. 65:201–12
    [Google Scholar]
  171. 171.
    von Frisch K. 1967. The Dance Language and Orientation of Bees Cambridge, MA: Belknap
  172. 172.
    Vossler F 2022. Large-scale breeding of stingless bees: a plea for sustainable stingless bee keeping and native bee-plant-forest conservation in the Chaco region of South America (Hymenoptera, Apidae, Meliponini). Pot-Propolis in Stingless Bee Ecology P Vit, V Bankova, M Popova, DW Roubik Berlin: Springer. In press
    [Google Scholar]
  173. 173.
    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 41:428–35
    [Google Scholar]
  174. 174.
    Wang S, Wittwer B, Heard TA, Goodger JQ, Elgar MA. 2018. Nonvolatile chemicals provide a nest defence mechanism for stingless bees Tetragonula carbonaria (Apidae, Meliponini). Ethology 124:633–40
    [Google Scholar]
  175. 175.
    Wille A. 1983. The biology of the stingless bees. Annu. Rev. Entomol. 28:41–64
    [Google Scholar]
  176. 176.
    Zheng H, Nishida A, Kwong WK, Koch H, Engel P et al. 2016. Metabolism of toxic sugars by strains of the bee gut symbiont Gilliamella apicola. mBio 7:e01326–16
    [Google Scholar]
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