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

Journal of Experimental Biology

Volumn 212, Issue 8, 2009, Pages 1153-1162

  Schorkopf, Dirk Louis P ^a   Hrncir, Michael ^a,b   Mateus, Sidnei ^b   Zucchi, Ronaldo ^b   Schmidt, Veronika M ^a   Barth, Friedrich G ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Agonistic behaviour; Communication; Eusocial bees; Semiochemicals; Trail substance

Indexed keywords

2 TRIDECANONE; 2-TRIDECANONE; ALDEHYDE; BENZALDEHYDE; BENZALDEHYDE DERIVATIVE; HEPTANOL; KETONE; NONANAL; PHEROMONE;

AGGRESSION; ANIMAL; ANIMAL COMMUNICATION; ARTICLE; BEE; CHEMISTRY; DRUG EFFECT; FEEDING BEHAVIOR; ISOLATION AND PURIFICATION; METABOLISM; PHYSIOLOGY; SECRETION; SPECIES DIFFERENCE;

AGGRESSION; ALDEHYDES; ANIMAL COMMUNICATION; ANIMALS; BEES; BENZALDEHYDES; FEEDING BEHAVIOR; HEPTANOL; KETONES; PHEROMONES; SPECIES SPECIFICITY;

APOIDEA; FORMICIDAE; ISOPTERA; MELIPONINAE; SCAPTOTRIGONA; TRIGONA SPINIPES;

EID: 63849192522     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.021113     Document Type: Article

References (71)

1. Abdalla, F. C. and da Cruz-Landim, C. (2001). Dufour glands in the hymenopterans (Apidae, Formicidae, Vespidae): a review. Braz. J. Biol. 61, 95-106.
2. Barrera-Gordillo, R. (2005). Secreción de las glándulas mandibulares de Scaptotrigona mexicana Guerin-Menewille (Hymenoptera: Meliponinae): Análisis químico y actividad biológica. University of Chiapas, Mexico.
3. Billen, J. (2006). Signal variety and communication in social insects. Proc. Neth. Entomol. Soc. Meet. 17, 9-25.
4. Blum, M. S. (1966). Chemical releasers of social behavior. VIII. Citral in the mandibular gland secretion of Lestrimelitta limao (Hymenoptera: Apoidea: Melittidae). Ann. Entomol. Soc. Am. 59, 962-964.
5. Blum, M. S. and Brand, J. M. (1972). Social insect pheromones: their chemistry and function. Am, Zool. 12, 553-576.
6. Blum, M. S., Crewe, R. M., Kerr, W. E., Keith, L. H., Garrison, A. W. and Walker, M. M. (1970). Citral in stingless bees: isolation and functions in trail-laying and robbing. J. Insect Physiol. 16, 1637-1648.
7. Camargo, J. M. F. and Pedro, S. R. M. (1992). Systematics, phylogeny and biogeography of the Meliponinae (Hymenoptera, Apinae): a mini-review. Apidologie 23, 509-522.
8. Camargo, J. M. F. and Pedro, S. R. M. (2007). Meliponini Lepeletier, 1836. In Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region (ed. J. S. Moure, D. Urban and G. A. R. Melo), pp. 272-578. Curitiba: Sociedade Brasileira de Entomologia.
9. Castro, P. R. C. (1975). Mutualismo entre Trigona spinipes (Fabricius, 1793) e Aethalion reticulatum (L, 1767) em Cajanus indicus Spreng. na presenca de Camponotus spp. Cienc. Cult. 27, 537-539.
10. Crane, E. (1990). Bees and Beekeeping. Ithaca, NY: Cornell University Press.
11. Cruz-López, L., Aguilar, S., Malo, E. A., Rincón, M., Guzman, M. and Rojas, J. C. (2007). Electroantennogram and behavioural responses of workers of the stingless bee Oxytrigona mediorufa to mandibular gland volatiles. Entomol. Exp. Appl. 123, 43-47.
12. da Cruz-Landim, C. (1967). Estudo comparativo de algumas glândulas das abelhas (Hymenoptera, Apoidea) e respectivas implicações evolutivas. Arq. Zool. 15, 177-290.
13. Eisner, T., Alsop, D., Hicks, K. and Meinwald, J. (1978). Defensive secretions of millipeds. In Handbook of Experimental Pharmacology Volume 48: Arthropod Venoms (ed. S. Bettini), pp. 41-72. Heidelberg: Springer.
14. Eisner, T., Eisner, M. and Siegler, M. (2005). Secret Weapons. London: Belknap Press.
15. Eltz, T., Brühl, C. A., van der Kaars, S. and Linsenmair, K. E. (2002). Determinants of stingless bee nest density in a lowland dipterocarp forest of Sabah, Malaysia. Oecologia 131, 27-34.
16. Engels, E., Engels, W., Schroder, W. and Francke, W. (1987). Intranidal worker reactions to volatile compounds identified from cephalic secretions in the stingless bee, Scaptotrigona postica (Hymenoptera, Meliponinae). J. Chem. Ecol. 13, 371-386.
17. Engels, E., Engels, W., Lübke, G., Schröder, W. and Francke, W. (1990). Volatile secretions of drones, queens and workers in relation to reproduction in the stingless bee, Scaptotrigona postica (Hymenopterea: Apidae, Trigonini). Entomol. Gen. 15, 91-101.
18. Francke, W. G., Lübke, G., Schröder, W., Reckziegel, A., Imperatriz-Fonseca, V., Kleinert, A., Engels, E., Hartfelder, K., Radtke, R. and Engels, W. (2000). Identification of oxygen containing volatiles in cephalic secretions of workers of Brazilian stingless bees. J. Braz. Chem. Soc. 11, 562-571.
19. Free, J. B. (1987). Pheromones of Social Bees. New York: Cornell University Press.
20. Gardner, A. and Grafen, A. (2009). Capturing the superorganism: a formal theory of group adaptation. J. Evol. Biol. DOI: 10.1111/j.1420-9101.2008.01681 .x
21. Haas, A. (1952). Die Mandibeldrüse als Duftorgan bei einigen Hymenopteren. Naturwissenschaften 39, 484.
22. Hölldobler, B. and Wilson, E. O. (1990). The Ants. Berlin: Springer.
23. Jarau, S., Hrncir, M., Zucchi, R. and Barth, F. G. (2000). Recruitment behaviour in stingless bees, Melipona scutellaris and M. quadrifasciata. I. Foraging at food sources differing in direction and distance. Apidologie 31, 81-91.
24. Jarau, S., Hrncir, M., Zucchi, R. and Barth, F. G. (2004). A stingless bee uses labial gland secretions for scent trail communication (Trigona recursa Smith 1863). J. Comp. Physiol. A 190, 233-239.
25. Jarau, S., Schulz, M., Hrncir, M., Francke, W., Zucchi, R., Barth, F. G. and Ayasse, M. (2006). Hexyl decanoate, the first trail pheromone compound identified in a stingless bee, Trigona recursa. J. Chem. Ecol. 32, 1555-1564.
26. Johnson, L. K. (1980). Alarm response of foraging Trigona fulviventris (Hymenoptera: Apidae) to mandibular gland components of competing bee species. J. Kans. Entomol. Soc. 53, 357-362.
27. Johnson, L. K. and Hubbell, S. P. (1974). Aggression and competition among stingless bees: field studies. Ecology 55, 120-127.
28. Johnson, L. K., Haynes, L. W., Carlson, M. A., Fortnum, H. A. and Gordgas, D. L. (1985). Alarm substances of the stingless bee, Trigona silvestriana. J. Chem. Ecol. 11, 409-416.
29. Kaib, M. (1999). Termites. In Pheromones of Non-Lepidopteran Insects Associated with Agricultural Plants (ed. J. Hardie and A. K. Minks), pp. 329-353. Oxon: CAB International.
30. Kaib, M. (2000). Chemical signals and communication in termites: a review. Mitt. Dtsch. Ges. Allg. Angew. Entomol. 11,211-218.
31. Keeping, M. G., Crewe, R. M. and Field, B. I. (1982). Mandibular gland secretions of the old world stingless bee, Trigona gribodoi Magretti: isolation, identification, and compositional changes with age. J. Apic. Res. 21, 65-73.
32. Kerr, W. E. (1969). Some aspects of the evolution of social bees (Apidae). Evol. Behav.3, 119-175.
33. Kerr, W. E. and da Cruz, C. C. (1961). Funções diferentes tomadas pela glândula mandibular na evolução das abelhas em geral e em Trigona (Oxytrigona) tataira em especial. Rev. Bras. Biol. 21, 1-16.
34. Kerr, W. E., Blum, M. and Fales, H. M. (1981). Communication of food source between workers of Trigona (Trigona) spinipes. Rev. Bras. Biol. 41, 619-623.
35. Kullenberg, B. (1973). Field experiments with chemical attractants on aculeate Hymenoptera males II. Zoon Suppl. 1, 31-42.
36. Kullenberg, B., Bergstöm, G., Bringer, B., Carlberg, B. and Cederberg, B. (1973). Observation on scent marking by Bombus Latr. and Psithyrus Lep. Males (Hym., Apidae) and Localization of Site of Production of the Secretion. Zoon Suppl. 1, 23-30.
37. Latreille, P. A. (1807). Genera Crustaceorum et Insectorum secundum ordinem naturalem in familias disposita, inconibus exemplisque plurimis explicata. Volume 3. Paris: Armand Koenig.
38. Lehmberg, L., Dworschak, K. and Blüthgen, N. (2008). Defensive behavior and chemical deterrence against ants in the stingless bee genus Trigona (Apidae, Meliponini). J. Apic. Res. 47, 17-21.
39. Leuthold, R. H. and Schlunegger, U. (1973). The alarm behaviour from the mandibular gland secretion in the ant Crematogaster scutellaris. Insectes Soc. 20, 205-214.
40. Lindauer, M. and Kerr, W. E. (1958). Die gegenseitige Verständigung bei den stachellosen Bienen. Z Vgl. Physiol. 41, 405-434.
41. Lindauer, M. and Kerr, W. E. (1960). Communication between the workers of stingless bees. Bee World 41, 29-41; 65-71.
42. Luby, J. M., Regnier, F. E., Clarke, E. T., Weaver, E. C. and Weaver, N. (1973). Volatile cephalic substances of the stingless bees Trionga mexicana and Trigona pectoralis. J. Insect Physiol. 19, 1111 -1127.
43. Maschwitz, U. (1964). Gefahrenalarmstoffe und Gefahrenalarmierung bei sozialen Hymenopteren. Z Vgl. Physiol. 47, 596-655.
44. Maynard Smith, J. and Harper, D. (2003). Animal Signals. Oxford: Oxford University Press.
45. McLafferty, F. and Stauffer, D. B. (1989). The Wiley/NBS Registry of Mass Spectral Data. New York: Wiley Interscience.
46. Michener, C. (1974). The Social Behavior of the Bees. Cambridge, MA: Harvard University Press.
47. Michener, C. (2000). The Bees of the World. Baltimore, MD: Johns Hopkins University Press.
48. Moure, J. S. (1942). Abelhas de Salobra (Hym. Apoidea). Papeís Avulsos 2, 291-321.
49. Nagamitsu, T. and Inoue, T. (1997). Aggressive foraging of social bees as a mechanism of floral resource partitioning in an Asian tropical rainforest. Oecologia 110, 432-439.
50. Nedel, J. O. (1960). Morphologie und Physiologie der Mandibeldrüse einiger Bienen- Arten (Apidae). Z Morphol. Ökol. Tiere 49, 139-183.
51. Nieh, J. C. (2004). Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie35, 159-182.
52. Nieh, J. C., Contrera, F. A. L. and Nogueira-Neto, P. (2003). Pulsed massrecruitment by a stingless bee, Trigona hyalinata. Proc. Biol. Sci. 270, 2191-2196.
53. Nogueira-Neto, P. (1997). Vida e criação de abelhas indígenas sem ferrão. São Paulo: Editora Nogueirapis.
54. Reeve, H. K. and Hölldobler, B. (2007). The emergence of a superorganism through intergroup competition. Proc. Natl. Acad. Sci. USA 104, 9736-9740.
55. Roubik, D. W. (1989). Ecology and Natural History of Tropical Bees. New York: Cambridge University Press.
56. Roubik, D. W. (2006). Stingless bee nesting biology. Apidologie 37, 124-143.
57. Roubik, D. W., Smith, B. H. and Carlson, R. L. (1987). Formic acid in caustic cephalic secretions of stingless bee Oxytrigona (Hymenoptera:Apidae) . J. Chem. Ecol. 13, 1079-1086.
58. Schorkopf, D. L. P., Jarau, S., Francke, W., Twele, R., Zucchi, R., Hrncir, M., Schmidt, V. M., Ayasse, M. and Barth, F. G. (2007). Spitting out information: Trigona bees deposit saliva to signal resource locations. Proc. Biol. Sci. 274, 895- 898.
59. Schwarz, H. F. (1932). Stingless bees in combat; observations on Trigona pallida Latreille on Barro Colorado Island. Nat. Hist. 32, 552-554.
60. Seeley, T. D. (1989). The honey bee colony as a superorganism. Am. Sci. 77, 546- 553.
61. Slaa, E. J. (2003). Foraging Ecology of Stingless Bees: From Individual Behaviour to Community Ecology. Utrecht: Budde Elinkwijk.
62. Slaa, E. J. (2006). Population dynamics of a stingless bee community in the seasonal dry lowlands of Costa Rica. Insectes Soc. 53, 70-79.
63. Smith, B. H. and Roubik, D. W. (1983). Mandibular glands of stingless bees (Hymenoptera: Apidae): chemical analysis of their contents and biological function in two species of Melipona. J. Chem. Ecol. 9, 1465-1472.
64. Townsend, G. F. (1963). Benzaldehyde: a new repellent for driving bees. Bee World 44, 146-149.
65. Vander Meer, R. K., Breed, M., Espelie, K. E. and Winston, M. L. (1998). Pheromone Communication in Social Insects. Boulder: Westview Press.
66. Vander Meer, R. K., Banks, W. A. and Lofgren, C. S. (2000). Repellent for ants. U.S. Patent 6,071,973. Washington D.C., U.S. Patent and Trademark Office.
67. Weaver, N., Weaver, E. C. and Clarke, E. T. (1975). Reactions of five species of stingless bees to some volatile chemicals and to other species of bees. J. Insect Physiol. 21, 479-494.
68. Wilson, D. S. and Sober, E. (1989). Reviving the superorganism. J. Theor. Biol. 136, 337-356.
69. Wilson, E. O. and Hölldobler, B. (2005). Eusociality: origin and consequences. Proc. Natl. Acad. Sci. USA 102, 13367-13371.
70. Wongsiri, S., Suwannapong, G., Srisook, N. and Hepburn, R. (2006). Pheromones of Asian Honeybees (Apis andreneformis, Apis cerana, Apis dorsata and Apis florea). In XV Congress IUSSI Proceedings, 30 July-4 August, 2006. Washington DC: IUSSI.
71. Wyatt, T. (2003). Pheromones and Animal Behaviour. Cambridge: Cambridge University Press.