Abstract
Stingless bees foraging for food improve recruitment by depositing chemical cues on valuable food sites or pheromone marks on vegetation. Using gas chromatography/mass spectrometry and bioassays, we showed that Melipona solani foragers leave a mixture composed mostly of long chain hydrocarbons from their abdominal cuticle plus methyl oleate from the labial gland as a scent mark on rich food sites. The composition of hydrocarbons was highly variable among individuals and varied in proportions, depending on the body part. A wide ratio of compounds present in different body parts of the bees elicited electroantennogram responses from foragers and these responses were dose dependent. Generally, in bioassays, these bees prefer to visit previously visited feeders and feeders marked with extracts from any body part of conspecifics. The mean number of visits to a feeder was enhanced when synthetic methyl oleate was added. We propose that this could be a case of multi-source odor marking, in which hydrocarbons, found in large abundance, act as a signature mixture with attraction enhanced through deposition of methyl oleate, which may indicate a rich food source.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aguilar I, Sommeijer M (2001) The deposition of anal excretions by Melipona favosa foragers (Apidae: Meliponinae): behavioural observations concerning the location of food sources. Apidologie 32:37–48. https://doi.org/10.1051/apido:2001109
Amano K, Nemoto T, Heard T (2000) What are stingless bees and why and how to use in crop pollination? A review. Japan Agricultural Research Quarterly 34:183–190
Araújo E, Costa M, Chaud-Netto J, Fowler H (2004) Body size and flight distance in stingles bees (Hymenoptera: Meliponini): inference of flight range and possible ecological implicatons. Braz J Biol 64:563–568. https://doi.org/10.1590/S1519-69842004000400003
Ascher JS, Pickering J (2017) Discover life: bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila) http://www.discoverlife.org/mp/20q?guide=Apoidea_species&flags=HAS. Accessed 6 July 2017
Ayala R, Gonzalez V, Engel M (2013) Mexican stingless bees (Hymenoptera: Apidae): diversity, distribution, and indigenous knowledge. In: Vit P, Pedro S, Roubik D (eds) Pot-honey a legacy of stingless bees, 1st edn. Springer, New York, pp 135–152
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. https://doi.org/10.1007/s00359-008-0321-7
Boogert N, Hofstede F, Aguilar I (2006) The use of food source scent marks by the stingless bee Trigona corvina (Hymenoptera: Apidae): the importance of the depositor’s identity. Apidologie 37:366–375. https://doi.org/10.1051/apido:2006001
Borges A, Ferreira-Caliman M, Nascimento F, Campos L, Tavares M (2012) Characterization of cuticular hydrocarbons of diploid and haploid males, workers and queens of the stingless bee Melipona quadrifasciata. Insect Soc 59:479–486. https://doi.org/10.1007/s00040-012-0242-x
Box G, Cox D (1964) An analysis of transformations. J Roy Stat Soc B Met 26:211–252. https://doi.org/10.2307/2287791
Ferreira-Caliman M, Nascimento F, Turatti I, Mateus S, Lopes N, Zucchi R (2010) The cuticular hydrocarbons profiles in the stingless bee Melipona marginata reflect task-related differences. J Insect Physiol 56:800–804. https://doi.org/10.1016/j.jinsphys.2010.02.004
Ferreira-Caliman M, Zucchi R, Nascimento F (2012) Cuticular hydrocarbons discriminate distinct colonies of Melipona marginata (Hymenoptera, Apinae, Meliponini). Sociobiology 59:1–12. 10.13102/sociobiology.v59i3.881
Ferreira-Caliman M, Falcon T, Mateus S, Zucchi R, Nascimento F (2013) Chemical identity of recently emerged workers, males, and queens in the stingless bee Melipona marginata. Apidologie 44:657–665. https://doi.org/10.1007/s13592-013-0214-9
Goulson D, Hawson S, Stout J (1998) Foraging bumblebees avoid flowers already visited by conspecifics or by other bumblebee species. Anim Behav 55:199–206. https://doi.org/10.1006/anbe.1997.0570
Goulson D, Stout J, Langley J, Hughes W (2000) Identity and function of scent marks deposited by foraging bumblebees. J Chem Ecol 26:2897–2911. https://doi.org/10.1023/A:1026406330348
Goulson D, Chapman JW, Hughes WOH (2001) Discrimination of unrewarding flowers by bees; direct detection of rewards and use of repellent scent marks. J Insect Behav 14:669–678. https://doi.org/10.1023/A:1012231419067
Greenleaf S, Williams N, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596. https://doi.org/10.1007/s00442-007-0752-9
Hrncir M, Jarau S, Zucchi R, Barth F (2004) On the origin and properties of scent marks deposited at the food source by a stingless bee, Melipona seminigra. Apidologie 35:3–13. https://doi.org/10.1051/apido:2003069
Jaffe K, Issa S, Sainz-Borgo C (2012) Chemical recruitment for foraging in ants (Formicidae) and termites (Isoptera): a revealing comparison. Psyche 2012:1–11. https://doi.org/10.1155/2012/694910
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, 1st edn. CRC Press, Florida, pp 223–249
Jarau S, Hrncir M, Ayasse M, Schulz C, Francke W, Zucchi R, Barth F (2004a) A stingless bee (Melipona seminigra) marks food sources with a pheromone from its claw retractor tendons. J Chem Ecol 30:793–804. https://doi.org/10.1023/B:JOEC.0000028432.29759.ed
Jarau S, Hrncir M, Zucchi R, Barth FG (2004b) A stingless bee uses labial gland secretions for scent trail communication (Trigona recursa smith 1863). J Comp Physiol A 190:233–239. https://doi.org/10.1007/s00359-003-0489-9
Jarau S, Hrncir M, Zucchi R, Barth FG (2005) Morphology and structure of the tarsal glands of the stingless bee Melipona seminigra. Naturwissenschaften 92:147–150. https://doi.org/10.1007/s00114-004-0601-1
Jarau S, Dambacher J, Twele R, Aguila I, Francke W, Ayasse M (2010) The trail pheromone of a stingless bee, Trigona corvina (Hymenoptera, Apidae, Meliponini), varies between populations. Chem Senses 35:1–9. https://doi.org/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. https://doi.org/10.1007/s13592-011-0070-4
Leadbeater E, Chittka L (2011) Do inexperienced bumblebee foragers use scent marks as social information? Anim Cogn 14:915–919. https://doi.org/10.1007/s10071-011-0423-4
Leonhardt S (2017) Chemical ecology of stingless bees. J Chem Ecol 43:385–402. https://doi.org/10.1007/s10886-017-0837-9
Malo EA, Castrejón-Gómez V, Cruz-López L, Rojas JC (2004) Antennal sensilla and electrophysiological response of male and female Spodoptera frugiperda (Lepidoptera: Noctuidae) to conspecific sex pheromone and plant odors. Ann Entomol Soc Am 97:1273–1284. https://doi.org/10.1603/0013-8746(2004)097[1273:ASAERO]2.0.CO;2
Meléndez-Ramirez V, Meneses-Calvillo L, Kevan P (2013) Effects of human disturbance and habitat fragmentation on stingless bees. In: Vit P, Pedro S, Roubik D (eds) Pot honey: a legacy of stingless bees, first. Springer New York, New York, pp 269–282
Michener C (2007) The bees of the world, 2nd edn. The Johns Hoptkins University Press, Baltimore
Michener C (2013) The Meliponini. In: Vit P, Silva P, Roubik D (eds) Pot honey: a legacy of stingless bees, 1st edn. Springer-Verlag New York, New York, pp 3–17
Nehring V, Wyatt T, Ettorre P (2013) Noise in chemical communication. In: Brumm H (ed) Animal communication and noise. Springer, Berlin, pp 373–405
Nieh J (1998) The role of a scent beacon in the communication of food location by the stingless bee, Melipona panamica. Behav Ecol Sociobiol 43:47–58. https://doi.org/10.1007/s002650050465
Nieh J (2004) Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 35:159–182. https://doi.org/10.1051/apido:2004007
Nieh J, Ramírez S, Nogueira-Neto P (2003) Multi-source odor-marking of food by a stingless bee, Melipona mandacaia. Behav Ecol Sociobiol 53:578–586. https://doi.org/10.1007/s00265-003-0658-4
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 197:243–249. https://doi.org/10.1007/s00359-010-0605-6
Reichle C, Aguilar I, Ayasse M et al (2013) Learnt information in species-specific “trail pheromone” communication in stingless bees. Anim Behav 85:225–232. https://doi.org/10.1016/j.anbehav.2012.10.029
Roselino AC, Rodrigues AV, Hrncir M (2016) Stingless bees (Melipona scutellaris) learn to associate footprint cues at food sources with a specific reward context. J Comp Physiol A 202:657–666. https://doi.org/10.1007/s00359-016-1104-1
Sakia R (1992) The box-cox transformation technique: a review. Stat 41:169. https://doi.org/10.2307/2348250
Saleh N, Chittka L (2006) The importance of experience in the interpretation of conspecific chemical signals. Behav Ecol Sociobiol 61:215–220. https://doi.org/10.1007/s00265-006-0252-7
Saleh N, Ohashi K, Thomson J, Chittka L (2006) Facultative use of the repellent scent mark in foraging bumblebees: complex versus simple flowers. Anim Behav 71:847–854. https://doi.org/10.1016/j.anbehav.2005.06.014
Saleh N, Scott AG, Bryning GP, Chittka L (2007) Distinguishing signals and cues: bumblebees use general footprints to generate adaptive behaviour at flowers and nest. Arthropod Plant Interact 1:119–127. https://doi.org/10.1007/s11829-007-9011-6
Schmidt V, Zucchi R, Barth F (2005) Scent marks left by Nannotrigona testaceicornis at the feeding site: cues rather than signals. Apidologie 36:285–291. https://doi.org/10.1051/apido:2005002
Schmitt U, Bertsch A (1990) Do foraging bumblebees scent-mark food sources and does it matter? Oecologia 82:137–144. https://doi.org/10.1007/BF00318545
Schmitt T, Herzner G, Weckerle B et al (2007) Volatiles of foraging honeybees Apis mellifera (Hymenoptera: Apidae) and their potential role as semiochemicals. Apidologie 38:164–170. https://doi.org/10.1051/apido:2006067
Schorkopf D, Jarau S, Francke W et al (2007) Spitting out information: Trigona bees deposit saliva to signal resource locations. Proc R Soc B 274:895–898. https://doi.org/10.1098/rspb.2006.3766
Schorkopf D, Morawetx L, Bento J et al (2011) Pheromone paths attached to the substrate in meliponine bees: helpful but not obligatory for recruitment success. J Comp Physiol A 197:755–764. https://doi.org/10.1007/s00359-011-0638-5
Shibahara A, Yamamoto K, Kinoshita A, Anderson BL (2008) An improved method for preparing dimethyl disulfide adducts for GC/MS analysis. J Am Oil Chem Soc 85:93–94. https://doi.org/10.1007/s11746-007-1169-7
Stout J, Goulson D (2001) The use of conspecific and interspecific scent marks by foraging bumblebees and honeybees. Anim Behav 62:183–189. https://doi.org/10.1006/anbe.2001.1729
Tóth E, Queller D, Dollin A, Strassmann J (2004) Conflict over male parentage in stingless bees. Insect Soc 51:1–11. https://doi.org/10.1007/s00040-003-0707-z
Williams C (1998) The identity of the previous visitor influences flower rejection by nectar-collecting bees. Anim Behav 56:673–681. https://doi.org/10.1006/anbe.1998.0794
Wilms J, Eltz T (2008) Foraging scent marks of bumblebees: footprint cues rather than pheromone signals. Naturwissenchaften 95:149–153. https://doi.org/10.1007/s00114-007-0298-z
Witjes S, Eltz T (2007) Influence of scent deposits on flower choice: experiments in an artificial flower array with bumblebees. Apidologie 38:12–18. https://doi.org/10.1051/apido:2006048
Wyatt T (2010) Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. J Comp Physiol 196:685–700. https://doi.org/10.1007/s00359-010-0564-y
Wyatt T (2014) Introduction to chemical signaling in vertebrates and invertebrates. In: Mucignat-Caretta C (ed) Neurobiology of chemical communication, first. Taylor & Francis, Boca Raton, pp 1–22
Acknowledgments
Thanks are given to the National Council of Science and Technology CONACYT for scholarship to D. A. R. (CV/grant number: 387462/255265). We also thank Dr. Mauricio Maldonado (UNAM) for his comments on an earlier version of this manuscript. This study was supported by CONACYT INFR-2014-01(224846).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Alavez-Rosas, D., Malo, E.A., Guzmán, M.A. et al. The Stingless Bee Melipona solani Deposits a Signature Mixture and Methyl Oleate to Mark Valuable Food Sources. J Chem Ecol 43, 945–954 (2017). https://doi.org/10.1007/s10886-017-0886-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-017-0886-0