The Role of Landscapes and Landmarks in Bee Navigation: A Review
Abstract
:1. Introduction
1.1. What Are Landmarks?
1.2. How Have Landmarks Been Described?
1.3. Why Is It So Difficult to Define Landmarks?
1.4. A Proposed Definition for Landmarks
2. Representations of Space in Honeybees
3. Different Types of Navigation
3.1. Snapshots
3.2. Vectors
3.3. Features and the Sensory World of the Animal
3.4. Feature Hierarchies
4. Orientation Flights and Returning to Known Locations
5. Different Sensory Modalities
5.1. Olfaction
5.2. Magnetoreception and Mechanosensation of Electrical Charges
5.3. Multimodality
6. Landmarks in Other Insects
7. Neural Bases of Landmark Memory
8. Recent Findings and Future Directions
Author Contributions
Acknowledgments
Conflicts of Interest
References
- Bradbury, J.W.; Vehrencamp, S.L. Principles of Animal Communication; Sinauer Associates: Sunderland, MA, USA, 1998. [Google Scholar]
- Horridge, A. What Does the Honeybee See?: And How Do We Know? Australian National University Press: Canberra, Australia, 2009. [Google Scholar]
- O’Keefe, J.; Nadel, L. The Hippocampus as a Cognitive Map; Clarendon Press: Oxford, UK, 1978. [Google Scholar] [CrossRef]
- Collett, T.S. Landmark Learning and Guidance in Insects. Philos. Trans. R. Soc. Lond. B 1992, 337, 295–303. [Google Scholar] [CrossRef]
- Gillner, S.; Weiß, A.M.; Mallot, H.A. Visual Homing in the Absence of Feature-Based Landmark Information. Cognition 2008, 109, 105–122. [Google Scholar] [CrossRef] [PubMed]
- Freas, C.A.; Fleischmann, P.N.; Cheng, K. Experimental Ethology of Learning in Desert Ants: Becoming Expert Navigators. Behav. Process. 2019, 158, 181–191. [Google Scholar] [CrossRef] [PubMed]
- Knaden, M.; Graham, P. The Sensory Ecology of Ant Navigation: From Natural Environments to Neural Mechanisms. Annu. Rev. Entomol. 2016, 61, 63–76. [Google Scholar] [CrossRef] [Green Version]
- Tinbergen, N. Uber Die Orientierung Des Bienenwolfes (Philanthus Triangulum Fabr.). J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1932, 16, 305–334. [Google Scholar]
- Frisch, K.V. The Dance Language and Orientation of Bees; Belknap Press of Harvard University Press: Cambridge, MA, USA, 1967. [Google Scholar]
- Anderson, A.M. A Model for Landmark Learning in the Honey-Bee. J. Comp. Physiol. A 1977, 114, 335–355. [Google Scholar] [CrossRef]
- Cartwright, B.A.; Collett, T.S. Landmark Learning in Bees. J. Comp. Physiol. A 1983, 151, 521–543. [Google Scholar] [CrossRef]
- Towne, W.F.; Ritrovato, A.E.; Esposto, A.; Brown, D.F. Honeybees Use the Skyline in Orientation. J. Exp. Biol. 2017, 220, 2476–2485. [Google Scholar] [CrossRef]
- Degen, J.; Kirbach, A.; Reiter, L.; Lehmann, K.; Norton, P.; Storms, M.; Koblofsky, M.; Winter, S.; Georgieva, P.B.; Nguyen, H.; et al. Honeybees Learn Landscape Features during Exploratory Orientation Flights. Curr. Biol. 2016, 26, 2800–2804. [Google Scholar] [CrossRef] [Green Version]
- Avarguès-Weber, A.; Dyer, A.G.; Ferrah, N.; Giurfa, M. The Forest or the Trees: Preference for Global over Local Image Processing Is Reversed by Prior Experience in Honeybees. Proc. R. Soc. B Biol. Sci. 2015, 282. [Google Scholar] [CrossRef]
- Dyer, F.C.; Gould, J.L. Honey Bee Navigation: The Honey Bee’s Ability to Find Its Way Depends on a Hierarchy of Sophisticated Orientation Mechanisms. Am. Sci. 1983, 71, 587–597. [Google Scholar]
- Gagliardo, A.; Ioalè, P.; Savini, M.; Wild, J.M. Having the Nerve to Home: Trigeminal Magnetoreceptor versus Olfactory Mediation of Homing in Pigeons. J. Exp. Biol. 2006, 209, 2888–2892. [Google Scholar] [CrossRef] [PubMed]
- Dittman, A.H.; Quinn, T.P. Homing in Pacific Salmon: Mechanisms and Ecological Basis. J. Exp. Biol. 1996, 199, 83–91. [Google Scholar] [PubMed]
- Collett, M.; Harland, D.; Collett, T.S. The Use of Landmarks and Panoramic Context in the Performance of Local Vectors by Navigating Honeybees. J. Exp. Biol. 2002, 205, 807–814. [Google Scholar] [PubMed]
- Menzel, R.; Tison, L.; Fischer-Nakai, J.; Cheeseman, J.; Balbuena, M.S.; Chen, X.; Landgraf, T.; Petrasch, J.; Polster, J.; Greggers, U. Guidance of Navigating Honeybees by Learned Elongated Ground Structures. Front. Behav. Neurosci. 2019, 12, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Dyer, A.G.; Rosa, M.G.P.; Reser, D.H. Honeybees Can Recognise Images of Complex Natural Scenes for Use as Potential Landmarks. J. Exp. Biol. 2008, 211, 1180–1186. [Google Scholar] [CrossRef]
- Avarguès-Weber, A.; Portelli, G.; Benard, J.; Dyer, A.; Giurfa, M. Configural Processing Enables Discrimination and Categorization of Face-like Stimuli in Honeybees. J. Exp. Biol. 2010, 213, 593–601. [Google Scholar] [CrossRef]
- Huber, B.; Couvillon, P.A.; Bitterman, M.E. Place and Position Learning in Honeybees (Apis mellifera). J. Comp. Psychol. 1994, 108, 213–219. [Google Scholar] [CrossRef]
- Chittka, L.; Geiger, K.; Kunze, J.A.N. The Influences of Landmarks on Distance Estimation of Honey Bees. Anim. Behav. 1995, 50, 23–31. [Google Scholar] [CrossRef]
- Caduff, D.; Timpf, S. On the Assessment of Landmark Salience for Human Navigation. Cogn. Process. 2008, 9, 249–267. [Google Scholar] [CrossRef]
- Hertz, M. Die Organisation Des Optischen Feldes Bei Der Biene. III. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 1931, 14, 629–674. [Google Scholar] [CrossRef]
- Zeil, J. Visual Homing: An Insect Perspective. Curr. Opin. Neurobiol. 2012, 22, 285–293. [Google Scholar] [CrossRef] [PubMed]
- Dyer, F.C.; Gould, J.L. Honey Bee Orientation: A Backup System for Cloudy Days. Science 1981, 214, 1041–1042. [Google Scholar] [CrossRef] [PubMed]
- Frisch, K.V.; Lindauer, M. Himmel und erde in Konkurrenz bei der Orientierung der Bienen. Naturwissenschaften 1954, 41, 245–253. [Google Scholar] [CrossRef]
- Menzel, R.; Brandt, R.; Gumbert, A.; Komischke, B.; Kunze, J. Two Spatial Memories for Honeybee Navigation. Proc. R. Soc. B Biol. Sci. 2000, 267, 961–968. [Google Scholar] [CrossRef]
- Tolman, E.C. Cognitive Maps in Rats and Men. Image Environ. Cogn. Mapp. Spat. Behav. 1948, 27–50. [Google Scholar] [CrossRef]
- Menzel, R.; Kirbach, A.; Haass, W.D.; Fischer, B.; Fuchs, J.; Koblofsky, M.; Lehmann, K.; Reiter, L.; Meyer, H.; Nguyen, H.; et al. A Common Frame of Reference for Learned and Communicated Vectors in Honeybee Navigation. Curr. Biol. 2011, 21, 645–650. [Google Scholar] [CrossRef] [Green Version]
- Menzel, R.; Greggers, U. The Memory Structure of Navigation in Honeybees. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2015, 201, 547–561. [Google Scholar] [CrossRef]
- Bennett, A.T.D. Do Animals Have Cognitive Maps? J. Exp. Biol. 1996, 199, 219–224. [Google Scholar]
- Cheeseman, J.F.; Millar, C.D.; Greggers, U.; Lehmann, K.; Pawley, M.D.M.; Gallistel, C.R.; Warman, G.R.; Menzel, R. Way-Finding in Displaced Clock-Shifted Bees Proves Bees Use a Cognitive Map. Proc. Natl. Acad. Sci. USA 2014, 111, 8949–8954. [Google Scholar] [CrossRef]
- Gould, J.L. The Locale Map of Honey Bees: Do Insects Have Cognitive Maps? Science 1986, 232, 861–863. [Google Scholar] [CrossRef] [PubMed]
- Hoinville, T.; Wehner, R. Optimal Multiguidance Integration in Insect Navigation. Proc. Natl. Acad. Sci. USA 2018, 115, 2824–2829. [Google Scholar] [CrossRef] [PubMed]
- Cheung, A.; Collett, M.; Collett, T.S.; Dewar, A.; Dyer, F.; Graham, P.; Mangan, M.; Narendra, A.; Philippides, A.; Stürzl, W.; et al. Still No Convincing Evidence for Cognitive Map Use by Honeybees. Proc. Natl. Acad. Sci. USA 2014, 111, E4396–E4397. [Google Scholar] [CrossRef] [PubMed]
- Cheeseman, J.F.; Millar, C.D.; Greggers, U.; Lehmann, K.; Pawley, M.D.M.; Gallistel, C.R.; Warman, G.R.; Menzel, R. Reply to Cheung et al.: The Cognitive Map Hypothesis Remains the Best Interpretation of the Data in Honeybee Navigation. Proc. Natl. Acad. Sci. USA 2014, 111, 4398. [Google Scholar] [CrossRef]
- Warren, W.H. Non-Euclidean Navigation. J. Exp. Biol. 2019, 222. [Google Scholar] [CrossRef]
- Rohrseitz, K.; Tautz, J. Honey Bee Dance Communication: Waggle Run Direction Coded in Antennal Contacts? J. Comp. Physiol. A Sens. Neural Behav. Physiol. 1999, 184, 463–470. [Google Scholar] [CrossRef]
- Collett, M.; Chittka, L.; Collett, T.S. Spatial Memory in Insect Navigation. Curr. Biol. 2013, 23, R789–R800. [Google Scholar] [CrossRef] [Green Version]
- Zhang, S.W.; Lehrer, M.; Srinivasan, M.V. Honeybee Memory: Navigation by Associative Grouping and Recall of Visual Stimuli. Neurobiol. Learn. Mem. 1999, 72, 180–201. [Google Scholar] [CrossRef] [Green Version]
- Collett, T.S. Insect Navigation En Route to the Goal: Multiple Strategies for the Use of Landmarks. J. Exp. Biol. 1996, 199, 227–235. [Google Scholar]
- Judd, S.P.D.; Collett, T.S. Multiple Stored Views and Landmark Guidance in Ants. Nature 1998, 392, 710–714. [Google Scholar] [CrossRef]
- Pahl, M.; Zhu, H.; Pix, W.; Tautz, J.; Zhang, S. Circadian Timed Episodic-like Memory—A Bee Knows What to Do When, and Also Where. J. Exp. Biol. 2007, 210, 3559–3567. [Google Scholar] [CrossRef] [PubMed]
- Harris, R.A.; De Ibarra, N.H.; Graham, P.; Collett, T.S. Ant Navigation: Priming of Visual Route Memories. Nature 2005, 438, 302. [Google Scholar] [CrossRef] [PubMed]
- Collett, T.S.; Fry, S.N.; Wehner, R. Sequence Learning by Honeybees. J. Comp. Physiol. A 1993, 172, 693–706. [Google Scholar] [CrossRef]
- Srinivasan, M.V.; Zhang, S.W.; Bidwell, N.J. Visually Mediated Odometry in Honeybees. J. Exp. Biol. 1997, 200, 2513–2522. [Google Scholar]
- Dacke, M.; Srinivasan, M.V. Honeybee Navigation: Distance Estimation in the Third Dimension. J. Exp. Biol. 2007, 210 Pt 5, 845–853. [Google Scholar] [CrossRef]
- Collett, T.S.; Collett, M. Route-Segment Odometry and Its Interactions with Global Path-Integration. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2015, 201, 617–630. [Google Scholar] [CrossRef]
- Bolek, S.; Wittlinger, M.; Wolf, H. Establishing Food Site Vectors in Desert Ants. J. Exp. Biol. 2012, 215, 653–656. [Google Scholar] [CrossRef]
- Gould, J.L. Landmark Learning by Honey Bees. Anim. Behav. 1987, 35, 26–34. [Google Scholar] [CrossRef]
- Gould, J.L. Natural History of Honey Bee Learning. In The Biology of Learning; Marler, P., Terrace, H.S., Eds.; Springer: Berlin/Heidelberg, Germany, 1984; pp. 149–180. [Google Scholar]
- Lehrer, M. Looking All around: Honeybees Use Different Cues in Different Eye Regions. J. Exp. Biol. 1998, 201, 3275–3292. [Google Scholar]
- Gould, J.L.; Towne, W.F. Honey Bee Learning. Adv. Insect Phys. 1988, 20, 55–86. [Google Scholar] [CrossRef]
- Avarguès-Weber, A.; Deisig, N.; Giurfa, M. Visual cognition in social insects. Annu. Rev. Entomol. 2011, 56, 423–443. [Google Scholar] [CrossRef] [PubMed]
- Vladusich, T.; Hemmi, J.M.; Srinivasan, M.V.; Zeil, J. Interactions of Visual Odometry and Landmark Guidance during Food Search in Honeybees. J. Exp. Biol. 2005, 208, 4123–4135. [Google Scholar] [CrossRef] [PubMed]
- Kheradmand, B.; Cassano, J.; Gray, S.; Nieh, J.C. Influence of Visual Targets and Landmarks on Honey Bee Foraging and Waggle Dancing. Insect Sci. 2018, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Menzel, R.; Fuchs, J.; Nadler, L.; Weiss, B.; Kumbischinski, N.; Adebiyi, D.; Hartfil, S.; Greggers, U. Dominance of the Odometer over Serial Landmark Learning in Honeybee Navigation. Naturwissenschaften 2010, 97, 763–767. [Google Scholar] [CrossRef] [PubMed]
- Menzel, R.; Chittka, L.; Eichmüller, S.; Geiger, K.; Peitsch, D.; Knoll, P. Dominance of Celestial Cues over Landmarks Disproves Map-Like Orientation in Honey Bees. Z. Nat. C 1990, 45, 723–726. [Google Scholar] [CrossRef]
- De Marco, R.; Menzel, R. Encoding Spatial Information in the Waggle Dance. J. Exp. Biol. 2005, 208, 3885–3894. [Google Scholar] [CrossRef] [PubMed]
- Dyer, F.C.; Gill, M.; Sharbowski, J. Motivation and Vector Navigation in Honey Bees. Naturwissenschaften 2002, 89, 262–264. [Google Scholar] [CrossRef]
- Menzel, R.; Geiger, K.; Joerges, J.; Müller, U.; Chittka, L. Bees Travel Novel Homeward Routes by Integrating Separately Acquired Vector Memories. Anim. Behav. 1998, 55, 139–152. [Google Scholar] [CrossRef]
- Chittka, L.; Kunze, J.; Shipman, C.; Buchmann, S.L. The Significance of Landmarks for Path Integration in Homing Honeybee Foragers. Naturwissenschaften 1995, 82, 341–343. [Google Scholar] [CrossRef]
- Wehner, R.; Hoinville, T.; Cruse, H.; Cheng, K. Steering Intermediate Courses: Desert Ants Combine Information from Various Navigational Routines. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2016, 202, 459–472. [Google Scholar] [CrossRef]
- Becker, L. Untersuchungen Über Das Heimfindevermögen Der Bienen (Examinations on the Homing Behaviour of Bees). Z. Vgl. Physiol. 1958, 41, 1–25. [Google Scholar] [CrossRef]
- Lehrer, M. Bees Which Turn Back and Look. Naturwissenschaften 1991, 78, 274–276. [Google Scholar] [CrossRef]
- Gould, J.L. Timing of Landmark Learning by Honey Bees. J. Insect Behav. 1988, 1, 373–377. [Google Scholar] [CrossRef]
- Osborne, J.L.; Smith, A.; Clark, S.J.; Reynolds, D.R.; Barron, M.C.; Lim, K.S.; Reynolds, A.M. The Ontogeny of Bumblebee Flight Trajectories: From Naïve Explorers to Experienced Foragers. PLoS ONE 2013, 8. [Google Scholar] [CrossRef] [PubMed]
- Zeil, J.; Hofmann, M.I.; Chahl, J.S. Catchment Areas of Panoramic Snapshots in Outdoor Scenes. J. Opt. Soc. Am. A 2003, 20, 450. [Google Scholar] [CrossRef] [PubMed]
- Capaldi, E.A.; Dyer, F.C. The Role of Orientation Flights on Homing Performance in Honeybees. J. Exp. Biol. 1999, 202, 1655–1666. [Google Scholar]
- Lihoreau, M.; Ings, T.C.; Chittka, L.; Reynolds, A.M. Signatures of a Globally Optimal Searching Strategy in the Three-Dimensional Foraging Flights of Bumblebees. Sci. Rep. 2016, 6, 30401. [Google Scholar] [CrossRef]
- Zeil, J. Orientation Flights of Solitary Wasps (Cerceris; Sphecidae; Hymenoptera): II. Similarities between Orientation and Return Flights and the Use of Motion Parallax. J. Comp. Physiol. A Sens. Neural Behav. Physiol. 1993, 172, 207–222. [Google Scholar] [CrossRef]
- Lehrer, M.; Collett, T.S. Approaching and Departing Bees Learn Different Cues to the Distance of a Landmark. J. Comp. Physiol. A 1994, 175, 171–177. [Google Scholar] [CrossRef]
- Lehrer, M.; Bianco, G. The Turn-Back-and-Look Behaviour: Bee versus Robot. Biol. Cybern. 2000, 83, 211–229. [Google Scholar] [CrossRef]
- Collett, T.S.; Rees, J.A. View-Based Navigation in Hymenoptera: Multiple Strategies of Landmark Guidance in the Approach to a Feeder. J. Comp. Physiol. A Sens. Neural Behav. Physiol. 1997, 181, 47–58. [Google Scholar] [CrossRef]
- Lehrer, M. Small-Scale Navigation in the Honeybee: Active Acquisition of Visual Information about the Goal. J. Exp. Biol. 1996, 199, 253–261. [Google Scholar]
- Dittmar, L.; Stürzl, W.; Baird, E.; Boeddeker, N.; Egelhaaf, M. Goal Seeking in Honeybees: Matching of Optic Flow Snapshots? J. Exp. Biol. 2010, 213 Pt 17, 2913–2923. [Google Scholar] [CrossRef]
- Srinivasan, M.V.; Zhang, S.W.; Lehrer, M.; Collett, T.S. Honeybee Navigation En Route to the Goal: Visual Flight Control and Odometry. J. Exp. Biol. 1996, 199, 237–244. [Google Scholar] [PubMed]
- Reinhard, J.; Srinivasan, M.V.; Guez, D.; Zhang, S.W. Floral Scents Induce Recall of Navigational and Visual Memories in Honeybees. J. Exp. Biol. 2004, 207, 4371–4381. [Google Scholar] [CrossRef] [PubMed]
- Fernandez, P.C.; Farina, W.M. Changes in Food Source Profitability Affect Nasonov Gland Exposure in Honeybee Foragers Apis mellifera L. Insectes Soc. 2001, 48, 366–371. [Google Scholar] [CrossRef]
- Free, J.B.; Williams, I.H. Scent-Marking of Flowers by Honeybees. J. Apic. Res. 1983, 22, 86–90. [Google Scholar] [CrossRef]
- Jarau, S.; Hrncir, M.; Zucchi, R.; Barth, F.G. A Stingless Bee Uses Labial Gland Secretions for Scent Trail Communication (Trigona recursa Smith 1863). J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2004, 190, 233–239. [Google Scholar] [CrossRef] [PubMed]
- Lindauer, M.; Kerr, W. Communication between the Workers of Stingless Bees. Bee World 1960, 41, 29–41. [Google Scholar] [CrossRef]
- Jeanne, R.L. Chemical Communication during Swarm Emigration in the Social Wasp Polybia sericea (Olivier). Anim. Behav. 1981, 29, 102–113. [Google Scholar] [CrossRef]
- Hölldobler, B.; Wilson, E.O. The Ants; Harvard University Press: Cambridge, MA, USA, 1990. [Google Scholar]
- Steck, K.; Hansson, B.S.; Knaden, M. Smells like Home: Desert Ants, Cataglyphis fortis, Use Olfactory Landmarks to Pinpoint the Nest. Front. Zool. 2009, 6, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Clarke, D.; Whitney, H.; Sutton, G.; Robert, D. Detection and Learning of Floral Electric Fields by Bumblebees. Science 2013, 340, 66–69. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Greggers, U.; Koch, G.; Schmidt, V.; Dürr, A.; Floriou-Servou, A.; Piepenbrock, D.; Göpfert, M.C.; Menzel, R. Reception and Learning of Electric Fields in Bees. Proc. R. Soc. B Biol. Sci. 2013, 280. [Google Scholar] [CrossRef] [PubMed]
- Lihoreau, M.; Raine, N.E. Bee Positive: The Importance of Electroreception in Pollinator Cognitive Ecology. Front. Psychol. 2013. [Google Scholar] [CrossRef]
- Liang, C.H.; Chuang, C.L.; Jiang, J.A.; Yang, E.C. Magnetic Sensing through the Abdomen of the Honey Bee. Sci. Rep. 2016, 6, 23657. [Google Scholar] [CrossRef]
- Lambinet, V.; Hayden, M.E.; Reid, C.; Gries, G. Honey Bees Possess a Polarity-Sensitive Magnetoreceptor. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2017, 203, 1029–1036. [Google Scholar] [CrossRef]
- Martin, H.; Lindauer, M. The effect of the earth’s magnetic field on gravity orientation in the honey bee (Apis mellifica). J. Comp. Physiol. A 1977, 122, 145–187. [Google Scholar] [CrossRef]
- Walker, M.M.; Bitterman, M.E. Bitterman. Conditioned responding to magnetic fields by honeybees. J. Comp. Physiol. A 1985, 157, 67–71. [Google Scholar] [CrossRef]
- Ferrari, T.E. Magnets, Magnetic Field Fluctuations and Geomagnetic Disturbances Impair the Homing Ability of Honey Bees (Apis mellifera). J. Apic. Res. 2014, 53, 452–465. [Google Scholar] [CrossRef]
- Fleischmann, P.N.; Grob, R.; Müller, V.L.; Wehner, R.; Rössler, W. The Geomagnetic Field Is a Compass Cue in Cataglyphis Ant Navigation. Curr. Biol. 2018, 28, 1440–1444.e2. [Google Scholar] [CrossRef] [Green Version]
- Aron, S.; Beckers, R.; Deneubourg, J.L.; Pasteels, J.M. Memory and Chemical Communication in the Orientation of Two Mass-Recruiting Ant Species. Insectes Soc. 1993, 40, 369–380. [Google Scholar] [CrossRef]
- Buehlmann, C.; Hansson, B.S.; Knaden, M. Desert Ants Learn Vibration and Magnetic Landmarks. PLoS ONE 2012, 7. [Google Scholar] [CrossRef] [PubMed]
- Ostwald, M.M.; Shaffer, Z.; Pratt, S.C.; Fewell, J.H. Multimodal Cues Facilitate Nest Recognition in Carpenter Bee Aggregations. Anim. Behav. 2019, 155, 45–51. [Google Scholar] [CrossRef]
- Sánchez, D.; Nieh, J.C.; Vandame, R. Visual and Chemical Cues Provide Redundant Information in the Multimodal Recruitment System of the Stingless Bee Scaptotrigona mexicana (Apidae, Meliponini). Insectes Soc. 2011, 58, 575–579. [Google Scholar] [CrossRef]
- Kunze, J.; Gumbert, A. The Combined Effect of Color and Odor on Flower Choice Behavior of Bumble Bees in Flower Mimicry Systems. Behav. Ecol. 2000, 12, 447–456. [Google Scholar] [CrossRef]
- Lawson, D.A.; Chittka, L.; Whitney, H.M.; Rands, S.A. Bumblebees Distinguish Floral Scent Patterns, and Can Transfer These to Corresponding Visual Patterns. Proc. R. Soc. B Biol. Sci. 2018, 285. [Google Scholar] [CrossRef]
- Lauer, J.; Lindauer, M. Genetisch Fixierte Lerndisposition bei der Honigbiene. In Informationsaufnahme und Informationsverar Beitung im Lebenden Organismus; Akademie der Wissenschaften und der Literatur: Mainz, Germany, 1971; Volume 1, pp. 1–87. (In German) [Google Scholar]
- Couvillon, P.A.; Bitterman, M.E. Compound-Component and Conditional Discrimination of Colors and Odors by Honeybees: Further Tests of a Continuity Model. Anim. Learn. Behav. 1988, 16, 67–74. [Google Scholar] [CrossRef]
- Inouye, B.D. Use of Visual and Olfactory Cues for Individual Nest Hole Recognition by the Solitary Bee Epicharis metatarsalis (Apidae, Anthophorinae). J. Insect Behav. 2000, 13, 231–238. [Google Scholar] [CrossRef]
- Zeil, J.; Wittman, D. Landmark Orientation during the Approach to the Nest in the stingless bee Trigona (Tetragonisca) angustula (Apidae, Meliponinae). Insectes Soc. 1993, 389, 381–389. [Google Scholar] [CrossRef]
- Richter, M.R. Social Wasp (Hymenoptera: Vespidae) Foraging Behavior. Annu. Rev. Entomol. 2000, 45, 121–150. [Google Scholar] [CrossRef]
- Nieh, J.C. Recruitment Communication in Stingless Bees (Hymenoptera, Apidae, Meliponini). Apidologie 2004, 35, 159–182. [Google Scholar] [CrossRef]
- Nieh, J.C.; Contrera, F.A.L.; Yoon, R.R.; Barreto, L.S.; Imperatriz-Fonseca, V.L. Polarized Short Odor-Trail Recruitment Communication by a Stingless Bee, Trigona spinipes. Behav. Ecol. Sociobiol. 2004, 56, 435–448. [Google Scholar] [CrossRef]
- Ayasse, M.; Jarau, S. Chemical Ecology of Bumble Bees. Annu. Rev. Entomol. 2014, 59, 299–319. [Google Scholar] [CrossRef] [PubMed]
- Wehner, R.; Boyer, M.; Loertscher, F.; Sommer, S.; Menzi, U. Ant Navigation: One-Way Routes Rather than Maps. Curr. Biol. 2006, 16, 75–79. [Google Scholar] [CrossRef] [PubMed]
- Fukushi, T.; Wehner, R. Navigation in Wood Ants Formica japonica: Context Dependent Use of Landmarks. J. Exp. Biol. 2004, 207, 3431–3439. [Google Scholar] [CrossRef]
- Martin, K.A.C. A Brief History of the “Feature Detector”. Cereb. Cortex 1994, 4, 1–7. [Google Scholar] [CrossRef]
- Borst, A.; Haag, J.; Reiff, D.F. Fly Motion Vision. Annu. Rev. Neurosci. 2010, 33, 49–70. [Google Scholar] [CrossRef]
- Zeil, J.; Ribi, W.A.; Narendra, A. Polarisation Vision in Ants, Bees and Wasps. In Polarized Light and Polarization Vision in Animal Sciences; Horváth, G., Ed.; Springer: Berlin/Heidelberg, Germany, 2014; pp. 41–60. [Google Scholar] [CrossRef]
- Hempel de Ibarra, N.; Vorobyev, M.; Menzel, R. Mechanisms, Functions and Ecology of Colour Vision in the Honeybee. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2014, 200, 411–433. [Google Scholar] [CrossRef]
- Aurore, A.W.; Mota, T.; Giurfa, M. New Vistas on Honey Bee Vision. Apidologie 2012, 43, 244–268. [Google Scholar] [CrossRef]
- Paulk, A.C.; Phillips-Portillo, J.; Dacks, A.M.; Fellous, J.M.; Gronenberg, W. The Processing of Color, Motion, and Stimulus Timing Are Anatomically Segregated in the Bumblebee Brain. J. Neurosci. 2008, 28, 6319–6332. [Google Scholar] [CrossRef] [Green Version]
- Mota, T.; Gronenberg, W.; Giurfa, M.; Sandoz, J.C. Chromatic Processing in the Anterior Optic Tubercle of the Honey Bee Brain. J. Neurosci. 2013, 33, 4–16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mertes, M.; Dittmar, L.; Egelhaaf, M.; Boeddeker, N. Visual Motion-Sensitive Neurons in the Bumblebee Brain Convey Information about Landmarks during a Navigational Task. Front. Behav. Neurosci. 2014, 8, 335. [Google Scholar] [CrossRef] [PubMed]
- Plath, J.A.; Entler, B.V.; Kirkerud, N.H.; Schlegel, U.; Galizia, C.G.; Barron, A.B. Different Roles for Honey Bee Mushroom Bodies and Central Complex in Visual Learning of Colored Lights in an Aversive Conditioning Assay. Front. Behav. Neurosci. 2017, 11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Van Nest, B.N.; Wagner, A.E.; Marrs, G.S.; Fahrbach, S.E. Volume and Density of Microglomeruli in the Honey Bee Mushroom Bodies Do Not Predict Performance on a Foraging Task. Dev. Neurobiol. 2017, 77, 1057–1071. [Google Scholar] [CrossRef] [PubMed]
- Honkanen, A.; Adden, A.; Da Silva Freitas, J.; Heinze, S. The Insect Central Complex and the Neural Basis of Navigational Strategies. J. Exp. Biol. 2019, 222. [Google Scholar] [CrossRef] [PubMed]
- Seelig, J.D.; Jayaraman, V. Neural Dynamics for Landmark Orientation and Angular Path Integration. Nature 2015, 521, 186–191. [Google Scholar] [CrossRef] [PubMed]
- Paulk, A.C.; Dacks, A.M.; Phillips-Portillo, J.; Fellous, J.M.; Gronenberg, W. Visual Processing in the Central Bee Brain. J. Neurosci. 2009, 29, 9987–9999. [Google Scholar] [CrossRef] [Green Version]
- Zwaka, H.; Bartels, R.; Lehfeldt, S.; Jusyte, M.; Hantke, S.; Menzel, S.; Gora, J.; Alberdi, R.; Menzel, R. Learning and Its Neural Correlates in a Virtual Environment for Honeybees. Front. Behav. Neurosci. 2019, 12, 279. [Google Scholar] [CrossRef]
- Buatois, A.; Flumian, C.; Schultheiss, P.; Avarguès-Weber, A.; Giurfa, M. Transfer of Visual Learning between a Virtual and a Real Environment in Honey Bees: The Role of Active Vision. Front. Behav. Neurosci. 2018, 12, 139. [Google Scholar] [CrossRef]
- Olsson, S.B.; Kuebler, L.S.; Veit, D.; Steck, K.; Schmidt, A.; Knaden, M.; Hansson, B.S. A Novel Multicomponent Stimulus Device for Use in Olfactory Experiments. J. Neurosci. Methods 2011, 195, 1–9. [Google Scholar] [CrossRef]
- Rusch, C.; Roth, E.; Vinauger, C.; Riffell, J.A. Honeybees in a Virtual Reality Environment Learn Unique Combinations of Colour and Shape. J. Exp. Biol. 2017, 220, 4746. [Google Scholar] [CrossRef] [PubMed]
- Cope, A.J.; Sabo, C.; Vasilaki, E.; Barron, A.B.; Marshall, J.A.R. A Computational Model of the Integration of Landmarks and Motion in the Insect Central Complex. PLoS ONE 2017, 12, e0172325. [Google Scholar] [CrossRef] [PubMed]
- Müller, J.; Nawrot, M.; Menzel, R.; Landgraf, T. A Neural Network Model for Familiarity and Context Learning during Honeybee Foraging Flights. Biol. Cybern. 2018, 112, 113–126. [Google Scholar] [CrossRef] [PubMed]
- Ardin, P.; Peng, F.; Mangan, M.; Lagogiannis, K.; Webb, B. Using an Insect Mushroom Body Circuit to Encode Route Memory in Complex Natural Environments. PLoS Comput. Biol. 2016, 12, e1004683. [Google Scholar] [CrossRef]
- Zeil, J.; Boeddeker, N. Going Wild: Toward an Ecology of Visual Information Processing. In Invertebrate Neurobiology; North, G., Greenspan, R., Eds.; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, USA, 2007; Volume 2753, pp. 381–403. [Google Scholar]
- Boeddeker, N.; Mertes, M.; Dittmar, L.; Egelhaaf, M. Bumblebee Homing: The Fine Structure of Head Turning Movements. PLoS ONE 2015, 10, e0135020. [Google Scholar] [CrossRef] [PubMed]
- Benard, J.; Stach, S.; Giurfa, M. Categorization of Visual Stimuli in the Honeybee Apis mellifera. Anim. Cogn. 2006, 9, 257–270. [Google Scholar] [CrossRef]
- Stach, S.; Benard, J.; Giurfa, M. Local-Feature Assembling in Visual Pattern Recognition and Generalization in Honeybees. Nature 2004, 429, 758–761. [Google Scholar] [CrossRef]
- Evangelista, C.; Kraft, P.; Dacke, M.; Labhart, T.; Srinivasan, M.V. Honeybee Navigation: Critically Examining the Role of the Polarization Compass. Philos. Trans. R. Soc. B Biol. Sci. 2014, 369. [Google Scholar] [CrossRef]
- Dacke, M.; Srinivasan, M.V. Two Odometers in Honeybees? J. Exp. Biol. 2008, 211, 3281–3286. [Google Scholar] [CrossRef]
- Baddeley, B.; Graham, P.; Philippides, A.; Husbands, P. Holistic Visual Encoding of Ant-like Routes: Navigation without Waypoints. Adapt. Behav. 2011, 19, 3–15. [Google Scholar] [CrossRef]
- Wystrach, A.; Mangan, M.; Philippides, A.; Graham, P. Snapshots in Ants? New Interpretations of Paradigmatic Experiments. J. Exp. Biol. 2013, 216, 1766–1770. [Google Scholar] [CrossRef] [PubMed]
- Borst, A.; Helmstaedter, M. Common Circuit Design in Fly and Mammalian Motion Vision. Nat. Neurosci. 2015, 18, 1067–1076. [Google Scholar] [CrossRef] [PubMed]
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Kheradmand, B.; Nieh, J.C. The Role of Landscapes and Landmarks in Bee Navigation: A Review. Insects 2019, 10, 342. https://doi.org/10.3390/insects10100342
Kheradmand B, Nieh JC. The Role of Landscapes and Landmarks in Bee Navigation: A Review. Insects. 2019; 10(10):342. https://doi.org/10.3390/insects10100342
Chicago/Turabian StyleKheradmand, Bahram, and James C. Nieh. 2019. "The Role of Landscapes and Landmarks in Bee Navigation: A Review" Insects 10, no. 10: 342. https://doi.org/10.3390/insects10100342