Skip to main content
Log in

Stingless bees (Melipona scutellaris) learn to associate footprint cues at food sources with a specific reward context

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Foraging insects leave chemical footprints on flowers that subsequent foragers may use as indicators for recent flower visits and, thus, potential resource depletion. Accordingly, foragers should reject food sources presenting these chemical cues. Contrasting this assumption, experimental studies in stingless bees (Apidae, Meliponini), so far, demonstrated an attractive effect of footprints. These findings lead to doubts about the meaning of these chemical cues in natural foraging contexts. Here, we asked whether foragers of stingless bees (Melipona scutellaris) use footprints according to the previously experienced reward level of visited food sources. Bees were trained to artificial flower patches, at which the reward of a flower either decreased or, alternatively, increased after a visit by a forager. Individuals were allowed a total of nine foraging bouts to the patch, after which their preference for visited or unvisited flowers was tested. In the choice tests, bees trained under the decreasing reward context preferred unvisited flowers, whereas individuals trained under the increasing reward context preferred visited flowers. Foragers without experience chose randomly between visited and unvisited flowers. These results demonstrate that M. scutellaris learns to associate unspecific footprint cues at food sources with differential, specific reward contexts, and uses these chemical cues accordingly for their foraging decisions.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • 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

    Article  Google Scholar 

  • Best LS, Bierzychudek P (1982) Pollinator foraging on foxglove (Digitalis purpurea): a test of a new model. Evolution 36:70–79

    Article  Google Scholar 

  • Biesmeijer JC, Slaa EJ (2006) The structure of eusocial bee assemblages in Brazil. Apidologie 37:240–258

    Article  Google Scholar 

  • Camargo JMF, Pedro SRM (2013) Meliponini Lepeletier, 1836. In: Moure JS, Urban D, Melo GAR (eds) Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region—online version. Available at http://www.moure.cria.org.br/catalogue. Accessed Mar/15/2015

  • Castellanos MC, Wilson P, Thomson JD (2002) Dynamic nectar replenishment in flowers of Penstemon (Scrophulariaceae). Am J Bot 89:111–118

    Article  PubMed  Google Scholar 

  • Clarke D, Whitney H, Sutton G, Robert D (2013) Detection and learning of floral electric fields by bumblebees. Science 340:66–69

    Article  CAS  PubMed  Google Scholar 

  • Colin ME, Richard D, Chauzy S (1991) Measurement of electric charges carried by bees: evidence of biological variations. J Bioelectricity 10:17–32

    Article  Google Scholar 

  • Drechsler P, Federle W (2006) Biomechanics of smooth adhesive pads in insects: influence of tarsal secretion on attachment performance. J Comp Physiol A 192:1213–1222

    Article  Google Scholar 

  • Eltz T (2006) Tracing pollinator footprints on natural flowers. J Chem Ecol 32:907–915

    Article  CAS  PubMed  Google Scholar 

  • Galetto L, Bernardello G (1992) Nectar secretion pattern and removal effects in six Argentinean Pitcairnioideae (Bromeliaceae). Bot Acta 105:292–299

    Article  Google Scholar 

  • Galetto L, Bernardello G (2004) Floral nectaries, nectar production dynamics and chemical composition in six Ipomoea species (Convolvulaceae) in relation to pollinators. Ann Bot 94:269–280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gawleta N, Zimmermann Y, Eltz T (2005) Repellent foraging recognition across bee families. Apidologie 36:325–330

    Article  Google Scholar 

  • Goulson D (2009) The use of scent marks by foraging bumble bees. In: Jarau S, Hrncir M (eds) Food exploitation by social insects—ecological, behavioral, and theoretical approaches. CRC-Press, Boca Raton, pp 251–260

    Chapter  Google Scholar 

  • Goulson D, Hawson SA, Stout JC (1998) Foraging bumblebees avoid flowers already visited by conspecifics or by other bumblebee species. Anim Behav 55:199–206

    Article  PubMed  Google Scholar 

  • Goulson D, Stout JC, Langley J, Hughes WOH (2000) Identity and function of scent marks deposited by foraging bumblebees. J Chem Ecol 26:2897–2911

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Guerenstein PG, Yepez AE, Van Haren J, Williams DG, Hildebrand JG (2004) Floral CO2 emission may indicate food abundance to nectar-feeding moths. Naturwissenschaften 91:329–333

    Article  CAS  PubMed  Google Scholar 

  • Harder LD (1983) Flower handling efficiency of bumble bees: morphological aspects of probing time. Oecologia 57:274–280

    Article  Google Scholar 

  • Harder LD (1985) Morphology as a predictor of flower choice by bumble bees. Ecology 66:198–210

    Article  Google Scholar 

  • Heinrich B (1976) Resource partitioning among some eusocial insects: bumblebees. Ecology 57:874–889

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Hrncir M, Maia-Silva C (2013) On the diversity of foraging-related traits in stingless bees. In: Vit P, Pedro SRM, Roubik D (eds) Pot-honey: a legacy of stingless bees. Springer, New York, pp 201–215

    Chapter  Google Scholar 

  • 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

    Google Scholar 

  • Hrncir M, Jarau S, Zucchi R, Barth FG (2004) On the origin and properties of scent marks deposited at the food source by a stingless bee, Melipona seminigra. Apidologie 35:3–13

    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, Boca Raton, pp 223–249

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • Jarau S, Hrncir M, Ayasse M, Schulz C, Francke W, Zucchi R, Barth FG (2004a) A stingless bee (Melipona seminigra) marks food sources with a pheromone from its claw retractor tendons. J Chem Ecol 30:793–804

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Johnson LK (1983) Foraging strategies and the structure of stingless bee communities in Costa Rica. In: Jaisson P (ed) Social insects in the tropics. Université Paris-Nord, Paris, pp 31–58

    Google Scholar 

  • Johnson LK, Hubbell SP (1975) Contrasting foraging strategies and coexistence of two bee species on a single resource. Ecology 56:1398–1406

    Article  Google Scholar 

  • Kato M (1988) Bumblebee visits to Impatiens spp.: pattern and efficiency. Oecologia 76:364–370

    Article  Google Scholar 

  • Leadbeater E, Chittka L (2011) Do inexperienced bumblebee foragers use scent marks as social information? Anim Cogn 14:915–919

    Article  PubMed  Google Scholar 

  • Leonhard AS, Dornhaus A, Papaj DR (2011) Forget-me-not: complex floral displays, inter-signal interactions, and pollinator cognition. Curr Zool 57:215–224

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lindauer M, Kerr WE (1958) Die gegenseitige Verständigung bei den stachellosen Bienen. Z Vergl Physiol 41:405–434

    Article  Google Scholar 

  • Lockey KH (1988) Lipids of the insect cuticle: origin, composition and function. Comp Biochem Physiol B 89:595–645

    Article  Google Scholar 

  • Lunau K (1996) Unidirectionality of floral colour changes. Pl Syst Evol 200:125–140

    Article  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 3–17

    Chapter  Google Scholar 

  • Nagamitsu T, Inoue T (1998) Interspecific morphological variation in stingless bees (Hymenoptera: apidae, Meliponinae) associated with floral shape and location in an Asian tropical rainforest. Entomol Sci 1:189–194

    Google Scholar 

  • Nieh JC (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

    Article  Google Scholar 

  • Nieh JC, Ramírez S, Nogueira-Neto P (2003) Multi-source odor-marking of food by a stingless bee, Melipona mandacaia. Behav Ecol Sociobiol 54:578–586

    Article  Google Scholar 

  • Nieh JC, Barreto LS, Contrera FAL, Imperatriz-Fonseca VL (2004) Olfactory eavesdropping by a competitively foraging stingless bee, Trigona spinipes. P Roy Soc Lond B Biol 271:1633–1640

    Article  Google Scholar 

  • Nogueira-Neto P (1997) Vida e criação de abelhas indígenas sem ferrão. Editora Nogueirapis, São Paulo

    Google Scholar 

  • Oberrath R, Böhning-Gaese K (1999) Floral colour change and the attraction of insect pollinators in lungwort (Pulmonaria collina). Oecologia 121:383–391

    Article  Google Scholar 

  • Pyke GH (1980) Optimal foraging in bumblebees: calculation of net rate of energy intake and optimal patch choice. Theor Popul Biol 17:232–246

    Article  CAS  PubMed  Google Scholar 

  • Reader T, MacLeod I, Elliott PT, Robinson OJ, Manica A (2005) Inter-order interactions between flower-visiting insects: foraging bees avoid flowers previously visited by hoverflies. J Insect Behav 18:51–57

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Roubik DW, Buchmann SL (1984) Nectar selection by Melipona and Apis mellifera (Hymenoptera: Apidae) and the ecology of nectar intake by bee colonies in a tropical forest. Oecologia 61:1–10

    Article  Google Scholar 

  • Saleh N, Chittka L (2006) The importance of experience in the interpretation of conspecific chemical signals. Behav Ecol Sociobiol 61:215–220

    Article  Google Scholar 

  • Saleh N, Ohashi K, Thomson JD, Chittka L (2006) Facultative use of the repellent scent mark in foraging bumblebees: complex versus simple flowers. Anim Behav 71:847–854

    Article  Google Scholar 

  • 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. Arth Plant Inter 1:119–127

    Article  Google Scholar 

  • Sánchez D, Nieh JC, Hénaut 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

    Article  PubMed  Google Scholar 

  • Schmidt VM, Zucchi R, Barth FG (2003) A stingless bee marks the feeding site in addition to the scent path (Scaptotrigona aff. depilis). Apidologie 34:237–248

    Article  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 

  • Schmitt U, Bertsch A (1990) Do foraging bumblebees scent-mark food sources and does it matter? Oecologia 82:137–144

    Article  Google Scholar 

  • 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. P Roy Soc B Biol Sci 274:895–898

    Article  Google Scholar 

  • Slaa EJ, Hughes WOH (2009) Local enhancement, local inhibition, eavesdropping, and the parasitism of social insect communication. In: Jarau S, Hrncir M (eds) Food exploitation by social insects—ecological, behavioral, and theoretical approaches. CRC-Press, Boca Raton, pp 147–164

    Chapter  Google Scholar 

  • Slaa EJ, Wassenberg J, Biesmeijer JC (2003) The use of field-based social information in eusocial foragers: local enhancement among nestmates and heterospecifics in stingless bees. Ecol Entomol 28:369–379

    Article  Google Scholar 

  • Stout JC, Goulson D (2001) The use of conspecific and interspecific scent marks by foraging bumblebees and honeybees. Anim Behav 62:183–189

    Article  Google Scholar 

  • Stout JC, Goulson D (2002) The influence of nectar secretion rates on the responses of bumblebees (Bombus spp.) to previously visited flowers. Behav Ecol Sociobiol 52:239–246

    Article  Google Scholar 

  • Stout JC, Goulson D, Allen JA (1998) Repellent scent-marking of flowers by a guild of foraging bumblebees (Bombus spp.). Behav Ecol Sociobiol 43:317–326

    Article  Google Scholar 

  • Suzuki MF, Ohashi K (2014) How does a floral colour-changing species differ from its non-colour-changing congener? A comparison of trait combinations and their effects on pollination. Funct Ecol 28:549–560

    Article  Google Scholar 

  • Villa JD, Weiss MR (1990) Observations of the use of visual and olfactory cues by Trigona spp. foragers. Apidologie 21:541–545

    Article  Google Scholar 

  • von Arx M, Goyret J, Davidowitz G, Raguso RA (2012) Floral humidity as a reliable sensory cue for profitability assessment by nectar-foraging hawkmoths. Proc Natl Acad Sci USA 109:9471–9476

    Article  Google Scholar 

  • Weiss MR (1991) Floral colour changes as cues for pollinators. Nature 354:227–229

    Article  Google Scholar 

  • Williams CS (1998) The identity of the previous visitor influences flower rejection by nectar-collecting bees. Anim Behav 56:673–681

    Article  PubMed  Google Scholar 

  • Wilms J, Eltz T (2008) Foraging scent marks of bumblebees: footprint cues rather than pheromone signals. Naturwissenschaften 95:149–153

    Article  CAS  PubMed  Google Scholar 

  • Witjes S, Eltz T (2007) Influence of scent deposits on flower choice: experiments in an artificial flower array with bumblebees. Apidologie 38:12–18

    Article  Google Scholar 

  • Witjes S, Eltz T (2009) Hydrocarbon footprints as a record of bumblebee flower visitation. J Chem Ecol 35:1320–1325

    Article  CAS  PubMed  Google Scholar 

  • Witjes S, Witsch K, Eltz T (2011) Reconstructing the pollinator community and predicting seed set from hydrocarbon footprints on flowers. Oecologia 165:1017–1029

    Article  PubMed  Google Scholar 

  • Yokoi T, Goulson D, Fujisaki K (2007) The use of heterospecific scent marks by the sweat bee Halictus aerarius. Naturwissenschaften 94:1021–1024

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Prof. Dr. Ronaldo Zucchi, for providing laboratory facilities and bee colonies necessary for this study, and the two anonymous referees, whose valuable comments and suggestions helped to improve our manuscript. This study complies with the current Brazilian law and was financially supported by the Brazilian funding agencies FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) under grants 08/58969-9 to AVR and 06/50809-7 to MH, and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) under grants 142905/2005-4 to ACR and 304722/2010-3 to MH.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael Hrncir.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Roselino, A.C., Rodrigues, A.V. & Hrncir, M. Stingless bees (Melipona scutellaris) learn to associate footprint cues at food sources with a specific reward context. J Comp Physiol A 202, 657–666 (2016). https://doi.org/10.1007/s00359-016-1104-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-016-1104-1

Keywords

Navigation