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Bee Positive: the Importance of Electroreception in Pollinator Cognitive Ecology

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Bee Positive: the Importance of Electroreception in Pollinator Cognitive Ecology GENERAL COMMENTARY published: 17 July 2013 doi: 10.3389/fpsyg.2013.00445 Bee positive: the importance of electroreception in pollinator cognitive ecology Mathieu Lihoreau 1*andNigelE.Raine2 1 School of Biological Sciences and the Charles Perkins Centre, The University of Sydney, Sydney, NSW, Australia 2 School of Biological Sciences, Royal Holloway University of London, Egham, Surrey, UK *Correspondence: [email protected] Edited by: Ken Cheng, Macquarie University, Australia Reviewed by: Björn Brembs, University of Regensburg, Germany A commentary on described how a bee visit temporarily figure-of-eight-shaped circuit performed modifies the electric charge of (Petunia) by foragers upon their return to the nest Detection and learning of floral electric flowers, suggesting that floral electric to communicate the location of rewarding fields by bumblebees properties could be used by future vis- flowers to nestmates (Von Frisch, 1967). byClarke,D.,Whitney,H.,Sutton,G.,and itors to assess the reward value without Comparison of electrical recordings to Robert, D. (2013). Science 340, 66–69. doi: necessarily needing to probe the flower. video clips of dancing bees revealed that 10.1126/science.1230883 To explore this possibility, the authors the sequence of wing beats and abdomen Reception and learning of electric fields in used differential conditioning in which movements performed by dancers gen- bees bees were trained to associate an electri- erates a specific modulated electric field by Greggers, U., Koch, G., Schmidt, V., cally charged feeder (30 V) with a sucrose composed of pulses of several hundred + Dürr, A., Floriou-Servou, A., Piepenbrock, reward (CS ) and an uncharged feeder volts. To test whether bees can detect and − D., Göpfert, M. C., and Menzel, R. (2013). with an aversive quinine solution (CS ). discriminate such electric cues, the team Proc. R. Soc. B 280:20130528. doi: 10.1098/ After extensive training (50 trials), bees stimulated tethered bees with either con- rspb.2013.0528 chose the rewarding feeder in around 80% stant or modulated electric fields. Stimuli of trials. Similar levels of performance mimicking those of a waggle dancer The global atmospheric circuit gener- were observed when bees were trained (among others) triggered both antennal ates a permanent electric field between with two feeders carrying the same charge movements and walking activity, suggest- the Earth surface and outer atmosphere but different electric field patterns (homo- ing that electric cues from conspecifics (Rycroft et al., 2000). The ground and geneous vs. bull’s eye shape), indicating evoke behavioral responses in a social con- plants conductively linked to it are neg- that these insects can learn both the mag- text. atively charged (Bowker and Crenshaw, nitude and geometry of an electric field. To identify the sensory receptors 2007), whereas animals build up positive Bees learned to perform even better in involved in electroreception the authors charge as they move in contact with air discrimination tasks if the two feeders dif- used proboscis extension response con- molecules (Jackson and McGonigle, 2005). fered both in color (shade of green) and ditioning, a classical paradigm to study Electric fields emanating from plants and their electric field pattern compared to if olfactory learning and memory (Tadeka, pollinators, such as bees, are believed to they differed only in color. Natural elec- 1961; Menzel, 2012). Harnessed honeybees promote pollination by enabling pollen tric fields around flowers may therefore were trained to associate an electrically grains to “jump” from flowers to pol- contribute to the multimodal sources of charged stimulus (CS+)withasucrose linators and vice versa (Corbet et al., information that bees use to learn and reward while an uncharged stimulus 1982). Two recent studies reveal that bees memorize floral rewards, in conjunction (CS−) was not rewarded. Whilst intact not only detect these electric fields but with color, pattern, shape, texture, humid- bees rapidly learned to discriminate the also learn to discriminate them, indicat- ity, or warmth (e.g., Stach et al., 2004; electrical stimulus, those whose anten- ing that electroreception should be seri- Dyer et al., 2006; Raine and Chittka, nae had either been removed or entirely ously considered alongside vision and 2008). coated with wax (to prevent move- olfaction when studying bee behavior and In another study published in the ment and block sensory receptors) were ecology. Proceedings of the Royal Society of London, unable to learn this cue. Interestingly, Writing in Science, Clarke et al. (2013) Greggers et al. (2013) went a step fur- if only the antennal articulations were demonstrated that bumblebees (Bombus ther asking both about the mechanisms free of wax, bees could detect vibra- terrestris) detect electric fields around of electroreception and their potential tions and were able to discriminate and plants and learn to use them to decide role in communication. They measured learn electrical cues to some extent. whether or not to visit flowers. Using the electric fields emanating from honey- Electrophysiological recordings of the a Faraday pail to measure electric fields bees (Apis mellifera)invariouscontexts, mechanosensory neurons in the Johnston’s generated by bees and plants, the team including during the “waggle dance”: the organ, a structure located in the second www.frontiersin.org July 2013 | Volume 4 | Article 445 | 1 Lihoreau and Raine Electroreception in pollinators antennal segment involved in detecting and route finding. Experimental manip- Jackson, C. W., Hunt, E., Sharkh, S., and Newland, P. acoustic vibrations (Ai, 2010), confirmed ulations of local electric fields in bees’ L. (2011). Static electric fields modify the locomo- that electric stimulation induces neu- foraging areas could test this hypothe- tory behaviour of cockroaches. J. Exp. Biol. 2014, 2020–2026. doi: 10.1242/jeb.053470 ronal responses. Therefore, much in the sis and help to clarify the importance Lihoreau, M., Chittka, L., and Raine, N. E. (2010). same way as body hairs are thought to of “electrical cognition” in these ani- Travel optimization by foraging bumblebees contribute to human electric field per- mals. through re-adjustments of traplines after discovery ception (Chapman et al., 2005), passive of new feeding locations. Am. Nat. 176, 744–757. antennal deflection caused by electrical ACKNOWLEDGMENTS doi: 10.1086/657042 Lihoreau, M., Raine, N. E., Reynolds, A. M., Stelzer, stimulation may activate mechanosensory This work was supported by an Australian R. J., Lim, K. S., Smith, A. D., et al. (2012). organs responsible for electroreception Research Council postdoctoral fellowship Radar tracking and motion-sensitive cameras in bees. to Mathieu Lihoreau. on flowers reveal the development of pollina- The observation that insects can sense tor multi-destination routes over large spatial electric fields is not new. Indeed, it scales. PLoS Biol. 10:e1001392. doi: 10.1371/jour- REFERENCES nal.pbio.1001392 Ai, H. (2010). Vibration-processing interneurons in has long been known that electric fields Menzel, R. (2012). The honeybee as a model for the honeybee brain. Front. Syst. Neurosci. 3:19. doi: induce a range of behavioral responses understanding the basis of cognition. Nat. Rev. 10.3389/neuro.06.019.2009 Neurosci. 13, 758–768. doi: 10.1038/nrn3357 in ants, cockroaches, mosquitoes, fruit Bowker, G. E., and Crenshaw, H. C. (2007). Newland, P. L., Hunt, E., Sharkh, S. M., Hama, N., flies, and bees [reviewed in Jackson et al. Electrostatic forces in wind-pollination Part 1: Takahata, M., and Jackson, C. (2008). Static elec- measurement of the electrostatic charge on (2011)]. However, previous studies have tric field detection and behavioural avoidance in pollen. Atmos. Environ. 41, 1587–1595. doi: typically focused on electric fields orders cockroaches. J. Exp. Biol. 211, 3682–3690. doi: 10.1016/j.atmosenv.2006.10.047 of magnitude stronger than those usually 10.1242/jeb.019901 Chapman,C.E.,Blondin,J.P.,Lapierre,A.M.,and Raine, N. E., and Chittka, L. (2008). The correlation found in nature, such as those generated Nguyen, D. H. (2005). Perception of local DC and of learning speed and natural foraging success in by high voltage power lines (Greenberg AC electric fields in humans. Bioelectromagnetics bumble-bees. Proc. R. Soc. B 275, 803–808. doi: 26, 357–366. doi: 10.1002/bem.20109 et al., 1981; Newland et al., 2008). By ques- 10.1098/rspb.2007.1652 Chittka, L., Geiger, K., and Kunze, J. (1995). The tioning the biological relevance of insect Rycroft, M. J., Israelsson, S., and Price, C. (2000). The influences of landmarks on distance estimation electroreception using ecologically real- global atmospheric electric circuit, solar activity of honey bees. Anim. Behav. 50, 23–31. doi: and climate change. J. Atmos. Sol. Terr. Phys. 62, istic electric cues, these recent observa- 10.1006/anbe.1995.0217 1563–1576. doi: 10.1016/S1364-6826(00)00112-7 tions on bees open a whole new window Clarke,D.,Whitney,H.,Sutton,G.,andRobert,D. Stach, S., Bernard, J., and Giurfa, M. (2004). Local- (2013). Detection and learning of floral electric into the study of insect sensory, cognitive, feature assembling in visual pattern recognition fields by bumblebees. Science 340, 66–69. doi: and behavioral ecology. Although nei- and generalization in honeybees. Nature 429, 10.1126/science.1230883 768–751. doi: 10.1038/nature02594 ther of these laboratory studies yet pro- Collett, T. S., and Baron, J. (1994). Biological com- Tadeka, K. (1961). Classical conditioned response in vide a clear answer about how bees actu- passes and the coordinate frame of landmark the honey bee. J. Insect Physiol. 6, 168–179. doi: ally detect and process electric fields, or memories in honeybees. Nature 368, 137–140. doi: 10.1016/0022-1910(61)90060-9 10.1038/368137a0 indeed whether electrical information is Von Frisch, K. (1967). The Dance Language and Corbet, S. A., Beament, J., and Eisikowitch, D. (1982). really used by bees under field conditions, Orientation of Bees. Cambridge, MA: Harvard Are electrostatic forces involved in pollen transfer? University Press.
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