Abstract
Foragers of several stingless bee species deposit attractive scent marks on solid substrates to precisely recruit nestmates to food. Interestingly, Partamona workers quickly recruit large numbers of nest mates to resources, likely even without the deposition of attractive scent marks. However, systematic studies of the recruitment system of these bees are lacking. We now studied the recruitment behavior of P. orizabaensis. Our findings show that foragers of this species can recruit large numbers of nestmates to food sources at a particular location. The precise nestmate recruitment does not rely on attractive scent marks deposited on substrates. We never observed any scent marking behavior and feeders baited with labial or mandibular gland extracts were not attractive for the bees. Chemical analyses showed that the foragers’ labial gland secretions exclusively contain long chain hydrocarbons, which render their role in recruitment communication unlikely. Whether mandibular gland secretions, which contain esters and alcohols that are known as attractive pheromones in other bee species, are used to guide recruits toward food during flight, remains elusive. We conclude that Partamona’s quick recruitment system that does not rely on conspicuous scent marks has evolved as a strategy against competition with sympatrically occurring and more aggressive bee species.
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References
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. doi:10.1051/apido:2005005
Ayasse M, Jarau S (2014) Chemical ecology of bumble bees. Annu Rev Entomol 59:299–319. doi:10.1146/annurev-ento-011613-161949
Barth FG, Hrncir M, Jarau S (2008) Signals and cues in the recruitment behavior of stingless bees (Meliponini). J Comp Physiol A 194:313–327. doi:10.1007/s00359-008-0321-7
Biesmeijer J, Slaa EJ (2004) Information flow and organization of stingless bee foraging. Apidologie 35:143–157. doi:10.1051/apido:2004003
Blum MS, Crewe RM, Kerr WE, Keith LH, Garrison AW, Walker MM (1970) Citral in stingless bees: isolation and functions in trail-laying and robbing. J Insect Physiol 16:1637–1648. doi:10.1016/0022-1910(70)90263-5
Brandley NC, Speiser DI, Johnsen S (2013) Eavesdropping on visual secrets. Evol Ecol 27:1045–1068. doi:10.1007/s10682-013-9656-9
Buser HR, Arn H, Guerin P, Rauscher S (1983) Determination of double bond position in mono-unsaturated acetates by mass spectrometry of dimethyl disulfide adducts. Anal Chem 55(6):818–822. doi:10.1021/ac00257a003
de Korte M, Weissenbacher KH, Crewe RM (1988) Chemical signals in a stingless bee Trigona (Meliplebeia) denoiti Vachal (Hymenoptera: apidae: Meliponinae). J Entmol Soc S Afr 51:9–16
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1):1–9
Hölldobler B, Wilson EO (1990) The ants. Springer, Berlin
Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393. doi:10.146/annurev.ento.50.071803.130359
Hrncir M (2009) Mobilizing the foraging force - mechanical signals in stingless bee recruitment. In: Jarau S, Hrncir M (eds) Food exploitation by social insects. Ecological, behavioral, and theoretical approaches. CRC Press, Boca Raton, pp 199–221
Hrncir M, Jarau S, Zucchi R, Barth FG (2000) Recruitment behavior in stingless bees, Melipona scutellaris and M. quadrifasciata II. Possible mechanisms of communication. Apidologie 31:93–113. doi:10.1051/apido:2000109
Hrncir M, Barth FG, Tautz J (2006a) Vibratory and airborne-sound signals in bee communication. In: Drosopoulos S, Claridge M (eds) Insect sounds and communication: physiology, behaviour, ecology, and evolution. CRC Press, Boca Raton, pp 421–436
Hrncir M, Schmidt VM, Schorkopf DLP, Jarau S, Zucchi R, Barth FG (2006b) Vibrating the food receivers: a direct way of signal transmission in bees (Melipona seminigra). J Comp Physiol A 192:879–887. doi:10.1007/s00359-006-0123-8
Jarau S (2009) Chemical communication during food exploitation in stingless bees. In: Jarau S, Hrncir M (eds) Food exploitation by social insects. Ecological, behavioral, and theoretical approaches. CRC Press, Boca Raton, pp 223–249
Jarau S, Hrncir M, Zucchi R, Barth FG (2000) Recruitment behavior in stingless bees, Melipona scutellaris and M. quadrifasciata. I. Foraging at food sources differing in direction and distance. Apidologie 31:81–91. doi:10.1051/apido:2000108
Jarau S, Hrncir M, Schmidt VM, Zucchi R, Barth FG (2003) Effectiveness of recruitment behavior in stingless bees (Apidae, Meliponini). Insect Soc 50:365–374. doi:10.1007/s00040-003-0684-2
Jarau S, Hrncir M, Zucchi R, Barth FG (2004) A stinglees bee uses labial gland secretions for scent trail communication (Trigona recursa Smith 1863). J Comp Physiol A 190:233–239. doi:10.1007/s00359-003-0489-9
Jarau S, Schulz CM, Hrncir M, Francke W, Zucchi R, Barth FG, Ayasse M (2006) Hexyl decanoate, the first trail pheromone compound identified in a stingless bee, Trgiona recursa. J Chem Ecol 32:1555–1564. doi:10.1007/s10886-006-9069-0
Jarau S, Dambacher J, Twele R, Aguilar I, Francke W, Ayasse M (2010) The trail pheromone of a stingless bee, Trigona corvina (Hymenoptera, Apidae, Meliponini), varies between populations. Chem Senses 35:593–601. doi:10.1093/chemse/bjq057
Jarau S, Hemmeter K, Aguilar I, Ayasse M (2011) A scientific note on trail pheromone communication in a stingless bee, Scaptotrigona pectoralis (Hymenoptera, Apidae, Meliponini). Apidologie 42:708–710. doi:10.1007/s13592-011-0070-4
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 59:527–532. doi:10.1007/s00040-012-0247-5
Johnson LK, Wiemer DF (1982) Nerol: an alarm substance of the stingless bee, Trigona fulviventris (Hymenoptera: apidae). J Chem Ecol 8:1167–1181. doi:10.1007/BF00990750
Johnson LK, Hayes LW, Carlson MA, Fortnum HA, Gorgas DL (1985) Alarm substances of stingless bee, Trigona silvestriana. J Chem Ecol 11:409–416. doi:10.1007/BF00989552
Keeping MG, Crewe RM, Field BI (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. doi:10.1080/00218839.1982.11100518
Keppner EM, Jarau S (2016) Influence of climatic factors on the flight activity and competition behavior of the stingless bee Partamona orizabaensis. J Comp Physiol A (this volume)
Kerr WE (1969) Some aspects of the evolution of social bees (Apidae). Evol Biol 3:119–175
Kerr WE, Ferreira A, De Mattos NS (1963) Communication among stingless bees-additional data (Hymenoptera: apidae). J NY Entomol Soc 71:80–90
Lichtenberg EM, Imperatriz-Fonseca VL, Nieh JC (2010) Behavioral suites mediate group-level foraging dynamics in communities of tropical stingless bees. Insect Soc 57:105–113. doi:10.1007/s00040-009-0055-8
Lichtenberg EM, Hrncir M, Turatti IC, Nieh JC (2011) Olfactory eavesdropping between two competing stingless bee species. Behav Ecol Sociobiol 65:763–774. doi:10.1007/s00265-010-1080-3
Lichtenberg EM, Graff Zivin J, Hrncir M, Nieh JC (2014) Eavesdropping selects for conspicuous signals. Curr Biol 24:R598–R599. doi:10.1016/j.cub.2014.05.062
Lindauer M, Kerr WE (1958) Die gegenseitige Verständigung bei den stachellosen Bienen. Z vergl Physiol 41:405–434. doi:10.1007/BF00344263
Lindauer M, Kerr WE (1960) Communication between the workers of stingless bees. Bee World 41:29–41. doi:10.1080/0005772X.1960.11095309
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. doi:10.1016/0022-1910(73)90036-X
Michener CD (2000) The bees of the world. Johns Hopkins University Press, Baltimore
Nieh JC (2004) Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 35:159–182. doi:10.1051/apido:2004007
Nieh JC, Contrera FAL, Nogueira-Neto P (2003) Pulsed mass-recruitment by a stingless bee, Trigona hyalinata. Proc R Soc London B 270:2191–2196. doi:10.1098/rspb.2003.2486
Nieh JC, Contrera FAL, Yoon RR, Barreto LS, Imperatriz-Fonseca VL (2004) Polarized short odor-trail recruitment communication by a stingless bee, Trigona spinipes. Behav Ecol Sociobiol 56:435–448. doi:10.1007/s00265-004-0804-7
Peake TM (2005) Eavesdropping in communication networks. In: McGregor PK (ed) Animal communication networks. Cambridge University Press, Cambridge, pp 13–37
R Development Core Team (2016) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna. http://www.R-project.org
Reichle C, Aguilar I, Ayasse M, Jarau S (2012) Stingless bees (Scaptotrigona pectoralis) learn foreign trail pheromones and use them to find food. J Comp Physiol A 197:243–249. doi:10.1007/s00359-010-0605-6
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 85:225–232. doi:10.1016/j.anbehav.2012.10.029
Sánchez D, Nieh JC, H énaut Y, Cruz L, Vandame R (2004) High precision during food recruitment of experienced (reactivated) foragers in the stingless bee Scaptotrigona mexicana (Apidae, Meliponini). Naturwissenschaften 91:346–349. doi:10.1007/s00114-004-0536-6
Schmidt VM, Zucchi R, Barth FG (2003) A stingless bee marks the feeding site in addition to the scent path (Scaptotriogna aff. depilis). Apidologie 34:237–248. doi:10.1051/apido:2003021
Schorkopf DLP, Jarau S, Francke W, Twele R, Zucchi R, Hrncir M, Schmidt VM, Ayasse M, Barth FG (2007) Spitting out information: trigona bees deposit saliva to signal resource locations. Proc R Soc B 274:895–898. doi:10.1098/rspb.2006.3766
Schorkopf DLP, Hrncir M, Mateus S, Zucchi R, Schmidt VM, Barth FG (2009) Mandibular gland secretions of meliponine worker bees: further evidence for their role in interspecific and intraspecific defence and aggression and against their role in food source signalling. J Exp Biol 212:1153–1162. doi:10.1242/jeb.021113
Schorkopf DLP, Morawetz L, Bento JMS, Zucchi R, Barth FG (2011) Pheromone paths attached to the substrate in meliponine bees: helpful but not obligatory for recruitment success. J Comp Physiol A 197:755–764. doi:10.1007/s00359-011-0638-5
Smith BH, Roubik DW (1983) Mandibular glands of stingless bees (Hymenoptera: apidae): chemical analysis of their contents and biological function in two species of Melipona. J Chem Ecol 9:1465–1472. doi:10.1007/BF00988512
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 19:13–19. doi:10.1007/s00049-009-0003-0
van Zweden JS, d’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. In: Blomquist GJ, Bagnères A-G (eds) Insect hydrocarbons. Biology, biochemistry, and chemical ecology. Cambridge University Press, Cambridge, pp 222–243
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 21:479–494. doi:10.1016/0022-1910(75)90153-5
Wilson EO (1971) The insect societies. Harvard University Press, Cambridge
Wyatt TD (2010) Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. J Comp Physiol A 196:685–700. doi:10.1007/s00359-010-0564-y
Wyatt TD (2014) Pheromones and animal behavior. Chemical signals and signatures, 2nd edn. Cambridge University Press, Cambridge
Acknowledgments
We thank the staff of the Tropical Field Station La Gamba of the University of Vienna in Costa Rica for accommodation and advice, as well as Eduardo Herrera González and Laura Winter for their enthusiasm and contributions to the field work. Likewise, we thank Javier Guevara Sequeira form the Ministerio del Ambiente y Energía (MINAE) in Costa Rica for his help in obtaining a research permit. Special thanks go to Masahiro Ryo for his help and advice regarding statistical analyses, as well as to Michael Hrncir and two anonymous reviewers for their valuable suggestion on an earlier manuscript version of this paper. Financial support was provided by a PROMOS scholarship from the German Academic Exchange Service (DAAD) awarded to I.C.F. and by the Deutsche Forschungsgemeinschaft (DFG project JA 1715/3-1).
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Flaig, I.C., Aguilar, I., Schmitt, T. et al. An unusual recruitment strategy in a mass-recruiting stingless bee, Partamona orizabaensis . J Comp Physiol A 202, 679–690 (2016). https://doi.org/10.1007/s00359-016-1111-2
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DOI: https://doi.org/10.1007/s00359-016-1111-2