Skip to main content
SpringerLink
Log in

Olfactory associative learning in two African stingless bee species (Meliponula ferruginea and M. bocandei, Meliponini)

  • Research Article
  • Published:
Insectes Sociaux Aims and scope Submit manuscript

Abstract

Worldwide only a few of the more than 500 stingless bee species has been studied in any detail. Most studies on stingless bees have been conducted in the Neotropics, whereas a very few have been undertaken in Africa. Foraging success is dependent to a greater or lesser extent on olfactory cues or signals. A prerequisite to effective foraging via odors is that the bees are able to associate odors with a nectar reward and memorize this information. In the context of olfactory learning, only five species of stingless bees have been studied using classical conditioning of the proboscis extension reflex (PER). Foragers are capable of using previously experienced olfactory information when choosing food sources, but they rarely respond in differential PER assays. This study examines for the first time the olfactory learning abilities of African stingless bees. A differential conditioning assay was used to study learning and memory of Meliponula ferruginea and Meliponula bocandei. Our results clearly show that both stingless bee species associate odors with a reward. Learning performance of both stingless bee species was poor compared to Apis m. scutellata. This might reflect that the experimental procedure has been optimized for Apis mellifera. However, the PER paradigm seems to be suitable to study learning, memory, and olfactory perception in Meliponula. As in honeybees, this paradigm will open the way to answer ecological, psychological, and neurobiological questions in these species.

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

Access this article

Log in via an institution

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abramson CI, Aquino IS, Stone SM (1999) Failure to find proboscis conditioning in one-day old Africanized honey bees (Apis mellifera L.) and in adult uruçu honey bees (Melipona scutellaris). J Comp Psychol 12:242–262

    Google Scholar 

  • Abramson CI, Mixson TA, Çakmak I, Place AJ, Wells H (2008) Pavlovian conditioning of the proboscis extension reflex in harnessed foragers using paired vs. unpaired and discrimination learning paradigms: tests for differences among honeybee subspecies in Turkey. Apidologie 39:428–435. doi:10.1051/apido:2008025

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Biesmeijer JC, Slaa EJ (2004) Information flow and organization of stingless bee foraging. Apidologie 35:143–157. doi:10.1051/apido:2004003

    Article  Google Scholar 

  • Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Physiol A 97:107–119

    CAS  Google Scholar 

  • Buchwald R, Breed MD (2005) Nestmate recognition cues in a stingless bee, Trigona fulviventris. Anim Behav 70:1331–1337. doi:10.1016/j.anbehav.2005.03.017

    Article  Google Scholar 

  • Couvillon MJ, Ratnieks FLW (2008) Odour transfer in stingless bee marmelada (Frieseomelitta varia) demonstrates that entrance guards use an “undesirable-absent” recognition system. Behav Ecol Sociobiol 21:194–201. doi:10.1007/s00265-007-0537-5

    CAS  Google Scholar 

  • Couvillon MJ, DeGrandi-Hoffman G, Gronenberg W (2010) Africanized honeybees are slower learners than their European counterparts. Naturwissenschaften 97:153–160. doi:10.1007/s00114-0090621-y

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cunningham JP, Moore CJ, Zalucki MP, West SA (2004) Learning, odour preference and flower foraging in moths. J Exp Biol 207:87–94. doi:10.1241/jeb.00733

    Article  PubMed  Google Scholar 

  • Eardley C (2004) Taxonomic revision of the African stingless bees (Apoidea: Apidae: Apinae: Meliponini). Afr Plant Prot 10:63–96

    Google Scholar 

  • Eardley C, Kwapong P (2013) Taxonomy as a tool for conservation of African stingless bees and their honey. In: Vit P, Pedro SRM, Roubik D (eds) Pot-honey a legacy of stingless bees. Springer, New York, pp 261–268

    Google Scholar 

  • Eltz T, Brühl CA, van der Kaars S, Chey VK, Linsenmair KE (2001) Pollen foraging and resource partitioning of stingless bees in relation to flowering dynamics in a Southeast Asian tropical rainforest. Insect Soc 48:273–279. doi:10.1007/PL00001777

    Article  Google Scholar 

  • Frost EH, Shutler D, Hillier NK (2011) Effects of cold immobilization and recovery period on honeybee learning, memory, and responsiveness to sucrose. J Insect Physiol 57:1385–1390. doi:10.1016/j.jinsphys.2011.07.001

    Article  CAS  PubMed  Google Scholar 

  • Giurfa M (2003) Cognitive neuroethology: dissecting non-elemental learning in a honeybee brain. Curr Opin Neurobiol 13:726–735. doi:10.1016/j.conb.2003.10.015

    Article  CAS  PubMed  Google Scholar 

  • Giurfa M, Sandoz JC (2012) Invertebrate learning and memory: fifty years of olfactory conditioning of the proboscis extension response in honeybees. Learn Mem 19:54–66. doi:10.1101/lm.024711.111

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • 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, Taylor and Francis Group. Bora Raton, pp 223–249

  • 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. doi:10.1007/s10886-010-9793-3

    Article  CAS  PubMed  Google Scholar 

  • Jones SM, van Zweden JS, Grüter C, Menezes C, Alves DA, Nunes-Silva P, Czaczkes T, Imperatriz-Fonseca VL, Ratnieks FLW (2011) The role of wax and resin in the nestmate recognition system of a stingless bee, Tetragonisca angustula. Behav Ecol Sociobiol 66:1–12. doi:10.1007/s00265-011-1246-7

    Article  Google Scholar 

  • Kajobe R (2006) Pollen foraging by Apis mellifera and stingless bees Meliponula bocandei and Meliponula nebulata in Bwindi Impenetrable National Park, Uganda. Afr J Ecol 45:265–274. doi:10.1111/j.1365-2028.2006.00701.x

    Article  Google Scholar 

  • Kajobe R, Echazarreta CM (2005) Temporal resource partitioning and climatological influences on colony flight and foraging of stingless bees (Apidae; Meliponini) in Ugandan tropical forests. Afr J Ecol 43:267–275. doi:10.1111/j.1365-2028.2005.00586.x

    Article  Google Scholar 

  • Kerr WE (1969) Some aspects of the evolution of social bees. Evol Biol 2:119–175

    Google Scholar 

  • Kiatoko N, Raina SK, Muli E, Mueke J (2014) Enhancement of fruit quality in Capsium annum through pollination by Hypotrigona gribo in Kakamega, Western Kenya. Entomol Sci 17:106–110. doi:10.1111/ens.12030

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Knudsen JT, Tollsten L, Bergström G (1993) Floral scents—a checklist of volatile compounds isolated by head-space techniques. Phytochem 33:253–280

    Article  CAS  Google Scholar 

  • Krausa K (2012) Populationsbiologische Untersuchungen an den afrikanischen Stachellosen Bienen Hypotrigona gribodoi und Liotrigona spec. Masterarbeit Ruhr-Universität Bochum

  • Kuwabara M (1957) Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifica. J Fac Sci Hokkaido Univ Ser VI Zool 13:458–464

    Google Scholar 

  • Laloi D, Sandoz JC, Picard-Nizou AL, Pham-Delègue MH (1999) Olfactory conditioning of the proboscis extension reflex in the bumble bee Bombus terrestris. Ann Soc Entomol 35:154–158

    Google Scholar 

  • Leonhardt SD, Heard TA, Wallace H (2014) Differences in the resource intake of two sympatric Australian stingless bee species. Apidologie 45:514–527. doi:10.1007/s13592-013-0266-x

    Article  Google Scholar 

  • Macharia JK, Raina SK, Muli EM (2007) Stingless bees in Kenya. Bees Dev J 83:9

    Google Scholar 

  • McCabe SI, Farina WM (2009) Odor information transfer in the stingless bee Melipona quadrifasciata: effect of in-hive experiences on classical conditioning of proboscis extension. J Comp Physiol A 195:113–122. doi:10.1007/s00359-008-0391-6

    Article  Google Scholar 

  • McCabe SI, Farina WM (2010) Olfactory learning in the stingless bee Tetragonisca angustula (Hymenoptera, Apidae, Meliponini). J Comp Physiol A 196:481–490. doi:10.1007/s00359-010-0536-2

    Article  CAS  Google Scholar 

  • McCabe SI, Hartfelder K, Santana WC, Farina WM (2007) Odor discrimination in classical conditioning of proboscis extension in two stingless bee species in comparison to Africanized honeybees. J Comp Physiol A 193:1089–1099. doi:10.1007/s00359-007-0260-8

    Article  CAS  Google Scholar 

  • McCabe SI, Hrncir M, Farina WM (2015) Vibrating donor-partners during trophallaxis modulate associative learning ability of food receivers in the stingless bee Melipona quadrifasciata. Learn Motiv. doi:10.1016/j.lmot.2014.10.005 (in press)

    Google Scholar 

  • Michener CD (1974) The social behavior of bees: A comparative study. Harvard University Press, Cambridge

    Google Scholar 

  • Michener CD (2013) The Meliponini. In: Vit P, Pedro SRM, Roubik D (eds) Pot-honey a legacy of stingless bees. Springer, New York, pp 3–18

    Google Scholar 

  • Nieh JC (2004) Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 35:159–182. doi:10.1051/apido:2004007

    Article  Google Scholar 

  • Nkoba K, Raina SK, Muli E, Mithöfer K, Mueke J (2012) Species richness and nest dispersion of some tropical meliponine bees (Apidae: Meliponinae) in six habitat types in the Kakamega forest, western Kenya. Int J Trop Insect Sci 32:194–202. doi:10.1017/S1742758412000355

    Article  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. doi:10.1016/j.anbehav.2010.11.020

    Article  Google Scholar 

  • Pham-Delègue MH, Bailez O, Blight MM, Masson C, Picard-Nizou AL, Wadhams LJ (1993) Behavioral discrimination of oilseed rape volatiles by the honeybee, Apis mellifera L. Chem Senses 18:483–494

    Article  Google Scholar 

  • Raina SK, Kioko E, Zethner O, Wren S (2011) Forest habitat conservation in Africa using commercially important insects. Annu Rev Entomol 56:465–485. doi:10.1146/annurev-ento-120709-1448085

    Article  CAS  PubMed  Google Scholar 

  • Reichle C, Jarau S, Aguilar I, Ayasse M (2010) Recruits of the stingless bee Scaptotrigona pectoralis learn food odors form the nest atmosphere. Naturwissenschaften 97:519–524. doi:10.1007/s00114-010-0662-2

    Article  CAS  PubMed  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 197:243–249. doi:10.1007/s00359-010-0605-6

    Article  CAS  Google Scholar 

  • Roselino AC, Hrncir M (2012) Repeated unrewarded scent exposure influences the food choice of stingless bee foragers, Melipona scutellaris. Anim Behav 83:755–762. doi:10.1016/j.anbehav.2011.12.025

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Schmidt VM, Zucchi R, Barth FG (2005) Scent marks left by Nannotrigona testaceicornis at the feeding site: cues rather than signals. Apidologie 36:285–291

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Singer TL (1998) Roles of hydrocarbons in the recognition system of insects. Amer Zool 38:394–405

    CAS  Google Scholar 

  • Takeda K (1961) Classical conditioned response in the honey bee. J Insect Physiol 6:168–179

    Article  CAS  Google Scholar 

  • Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A 157:263–277

    Article  CAS  PubMed  Google Scholar 

  • van Zweden JS, d’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. In: Blomquist GJ, Bagnéres AG (eds) Insect hydrocarbons. Biology, biochemistry and chemical ecology. Cambridge University Press

  • Vareschi E (1971) Duftunterscheidung bei der Honigbiene—Einzelzell-Ableitungen und Verhaltensreaktionen. Z vergl Physiol 75:143–173

    Google Scholar 

  • Watanabe H, Kobayashi Y, Sakura M, Matsumoto Y, Mizunami M (2003) Classical olfactory conditioning in the cockroach Periplaneta americana. Zoolog Sci 20:1447–1454. doi:10.2108/zsj.20.1447

    Article  PubMed  Google Scholar 

  • Wittmann D, Radtke R, Zeil J, Lübke 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 16:631–641

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank icipe—African Science for Food and Health, especially SK Raina for the strong support and the Kenyan Forest Service (KFS) for issuing research permits. Special thanks to the beekeepers from Ivihiga and Isiekuti. We are grateful to two anonymous reviewers for their helpful comments. JH was supported by the German Academic Exchange Service (DAAD) with travel grants, the Deutsche Studienstiftung supported KK with travel grants.

Author information

Authors and Affiliations

  1. Faculty of Biology and Biotechnology, Ruhr University Bochum, Universitätsstraße 150, 44801, Bochum, Germany

    J. Henske, K. Krausa, F. A. Hager & W. H. Kirchner

  2. African Bee Health Project, icipe-African Insect Science for Food and Health, PO Box 30772-00100, Nairobi, Kenya

    K. Nkoba

Authors
  1. J. Henske
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Krausa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. F. A. Hager
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. Nkoba
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. W. H. Kirchner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. Krausa.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Henske, J., Krausa, K., Hager, F.A. et al. Olfactory associative learning in two African stingless bee species (Meliponula ferruginea and M. bocandei, Meliponini). Insect. Soc. 62, 507–516 (2015). https://doi.org/10.1007/s00040-015-0430-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-015-0430-6

Keywords

Search

Navigation