Artículo

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" (2019) Frontiers in Behavioral Neuroscience. 12
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Elongated landscape features like forest edges, rivers, roads or boundaries of fields are particularly salient landmarks for navigating animals. Here, we ask how honeybees learn such structures and how they are used during their homing flights after being released at an unexpected location (catch-and-release paradigm). The experiments were performed in two landscapes that differed with respect to their overall structure: a rather feature-less landscape, and one rich in close and far distant landmarks. We tested three different forms of learning: learning during orientation flights, learning during training to a feeding site, and learning during homing flights after release at an unexpected site within the explored area. We found that bees use elongated ground structures, e.g., a field boundary separating two pastures close to the hive (Experiment 1), an irrigation channel (Experiment 2), a hedgerow along which the bees were trained (Experiment 3), a gravel road close to the hive and the feeder (Experiment 4), a path along an irrigation channel with its vegetation close to the feeder (Experiment 5) and a gravel road along which bees performed their homing flights (Experiment 6). Discrimination and generalization between the learned linear landmarks and similar ones in the test area depend on their object properties (irrigation channel, gravel road, hedgerow) and their compass orientation. We conclude that elongated ground structures are embedded into multiple landscape features indicating that memory of these linear structures is one component of bee navigation. Elongated structures interact and compete with other references. Object identification is an important part of this process. The objects are characterized not only by their appearance but also by their alignment in the compass. Their salience is highest if both components are close to what had been learned. High similarity in appearance can compensate for (partial) compass misalignment, and vice versa. © 2019 Menzel, Tison, Fischer-Nakai, Cheeseman, Balbuena, Chen, Landgraf, Petrasch, Polster and Greggers.

Registro:

Documento: Artículo
Título:Guidance of navigating honeybees by learned elongated ground structures
Autor:Menzel, R.; Tison, L.; Fischer-Nakai, J.; Cheeseman, J.; Balbuena, M.S.; Chen, X.; Landgraf, T.; Petrasch, J.; Polster, J.; Greggers, U.
Filiación:Institute of Biology, Freie Universität Berlin, Berlin, Germany
Fachbereich Biowissenschaften, Polytechnische Gesellschaft Frankfurt am Main, Institute für Bienenkunde, Goethe-Universität Frankfurt am Main, Frankfurt, Germany
Department of Anaesthesiology, Faculty of Medical and Health Science, The University of Auckland, Auckland, New Zealand
Laboratorio de Insectos Sociales, Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Instituto de Fisiología, Biología Molecular y Neurociencias (IFIBYNE), CONICET-Universidad de Buenos Aires, Buenos Aires, Argentina
Dahlem Center of Machine Learning and Robotics, Institute for Informatics, Freie Universität Berlin, Berlin, Germany
Palabras clave:Compass alignment; Ground structures; Guiding landmarks; Navigation; Object recognition; Sun compass; article; feeding; homing behavior; honeybee; landscape; learning; nonhuman; pasture; recognition; sun; vegetation
Año:2019
Volumen:12
DOI: http://dx.doi.org/10.3389/fnbeh.2018.00322
Título revista:Frontiers in Behavioral Neuroscience
Título revista abreviado:Front. Behav. Neurosci.
ISSN:16625153
Registro:http://digital.bl.fcen.uba.ar/collection/paper/document/paper_16625153_v12_n_p_Menzel

Referencias:

  • Able, K.P., Mechanisms of orientation, navigation and homing (1980) Animal Migration, Orientation, Navigation, pp. 281-387. , ed. S. A. Gauthreaux (New York, NY: Academic Press)
  • Ardin, P., Peng, F., Mangan, M., Lagogiannis, K., Webb, B., Using an insect mushroom body circuit to encode route memory in complex natural environments (2016) Plos Comput. Biol., 12
  • Balbuena, M.S., Tison, L., Hahn, M.L., Greggers, U., Menzel, R., Farina, W.M., Effects of sub-lethal doses of glyphosate on honeybee navigation (2015) J. Exp. Biol., 218, pp. 2799-2805
  • Barry, C., Lever, C., Hayman, R., Hartley, T., Burton, S., O’Keefe, J., The boundary vector cell model of place cell firing and spatial memory (2006) Rev. Neurosci., 17, pp. 71-97
  • Canny, J., A computational approach to edge detection (1986) IEEE Trans. Pattern Anal. Mach. Intell., 8, pp. 679-698
  • Chan, E., Baumann, O., Bellgrove, M.A., Mattingley, J.B., From objects to landmarks: The function of visual location information in spatial navigation (2012) Front. Psychol., 3, p. 304
  • Cheeseman, J.F., Millar, C.D., Greggers, U., Lehmann, K., Pawley, M.D., Gallistel, C.R., The cognitive map hypothesis remains the best interpretation of the data in honeybee navigation (2014) Proc. Natl. Acad. Sci. U S A, 111
  • Cheeseman, J.F., Millar, C.D., Greggers, U., Lehmann, K., Pawley, M.D., Gallistel, C.R., Way-finding in displaced clock-shifted bees proves bees use a cognitive map (2014) Proc. Natl. Acad. Sci. U S A, 111, pp. 8949-8954
  • Cheng, K., A purely geometric module in the rat’s spatial representation (1986) Cognition, 23, pp. 149-178
  • Cheng, K., Newcombe, N.S., Is there a geometric module for spatial orientation? Squaring theory and evidence (2005) Psychon. Bull. Rev., 12, pp. 1-23
  • Cheung, A., Collett, M., Collett, T.S., Dewar, A., Dyer, F., Graham, P., Still no convincing evidence for cognitive map use by honeybees (2014) Proc. Natl. Acad. Sci. U S A, 111, pp. E4396-E4397
  • Collett, T.S., Graham, P., Insect navigation: Do honeybees learn to follow highways? (2015) Curr. Biol., 25, pp. R240-R242
  • Degen, J., Kirbach, A., Reiter, L., Lehmann, K., Norton, P., Storms, M., Exploratory behaviour of honeybees during orientation flights (2015) Animal Behav, 102, pp. 45-57
  • Degen, J., Kirbach, A., Reiter, L., Lehmann, K., Norton, P., Storms, M., Honeybees learn landscape features during exploratory orientation flights (2016) Current Biology, 26, pp. 2800-2804
  • Dyer, F.C., Gould, J.L., Honey bee orientation: A backup system for cloudy days (1981) Science, 214, pp. 1041-1042
  • Fischer, J., Müller, T., Spatz, A.K., Greggers, U., Grünewald, B., Menzel, R., Neonicotinoids interfere with specific components of navigation in honeybees (2014) Plos One, 9
  • Furlan, A., Baldwin, T., Klippel, A., Landmark classification for route directions,’’ in Proceedings of the Fourth ACL-SIGSEM Workshop on Prepositions (Prague‎) (2007) Association for Computational Linguistics, pp. 9-16
  • Geva-Sagiv, M., Las, L., Yovel, Y., Ulanovsky, N., Spatial cognition in bats and rats: From sensory acquisition to multiscale maps and navigation (2015) Nat. Rev. Neurosci., 16, pp. 94-108
  • Geyr von Schweppenbug, H.V., Zur theorie der leitlinie (1933) Ardea, 22, pp. 83-92
  • Giger, G., (1996) Honeybee Vision: Analysis of Pattern Orientation, , Canberra: Australian National University
  • Guilford, T., Roberts, S., Biro, D., Rezek, I., Positional entropy during pigeon homing II: Navigational interpretation of Bayesian latent state models (2004) J. Theor. Biol., 227, pp. 25-38
  • Heithaus, E.R., Fleming, T.H., Opler, P.A., Foraging patterns and resource utilization in seven species of bats in a seasonal tropical forest (1975) Ecology, 56, pp. 841-854
  • Homberg, U., Heinze, S., Pfeiffer, K., Kinoshita, M., El Jundi, B., Central neural coding of sky polarization in insects (2011) Philos. Trans. R. Soc. Lond. B Biol. Sci., 366, pp. 680-687
  • Jacobs, L.F., Menzel, R., Navigation outside of the box: What the lab can learn from the field and what the field can learn from the lab (2014) Mov. Ecol., 2
  • Lipp, H.-P., Vyssotski, A.L., Wolfer, D.P., Renaudineau, S., Savini, M., Tröster, G., Pigeon homing along highways and exits (2004) Curr. Biol., 14, pp. 1239-1249
  • McNamara, T.P., Rump, B., Werner, S., Egocentric and geocentric frames of reference in memory of large-scale space (2003) Psychon. Bull. Rev., 10, pp. 589-595
  • Menzel, R., The cognitive structure of visual navigation in honeybees (2013) The New Visual Neuroscience, pp. 1179-1189. , eds J. S. Werner and L. M. Chalupa (Cambridge, MA: MIT Press)
  • Menzel, R., The insect mushroom body, an experience-dependent recoding device (2014) J. Physiol. Paris, 108, pp. 84-95
  • Menzel, R., Greggers, U., The memory structure of navigation in honeybees (2015) J. Comp. Physiol. a Neuroethol. Sens. Neural Behav. Physiol., 201, pp. 547-561
  • Menzel, R., Greggers, U., Smith, A., Berger, S., Brandt, R., Brunke, S., Honey bees navigate according to a map-like spatial memory (2005) Proc. Natl. Acad. Sci. U S A, 102, pp. 3040-3045
  • Menzel, R., Kirbach, A., Haass, W.-D., Fischer, B., Fuchs, J., Koblofsky, M., A common frame of reference for learned and communicated vectors in honeybee navigation (2011) Curr. Biol., 21, pp. 645-650
  • Moser, E.I., Moser, M.B., A metric for space (2008) Hippocampus, 18, pp. 1142-1156
  • Müller, J., Nawrot, M., Menzel, R., Landgraf, T., A neural network model for familiarity and context learning during honeybee foraging flights (2018) Biol. Cybern., 112, pp. 113-126
  • O’Keefe, J., Nadel, J., (1978) The Hippocampus as a Cognitive Map, , New York, NY: Oxford University Press
  • Osborne, J.L., Smith, A., Clark, S.J., Reynolds, D.R., Barron, M.C., Lim, K.S., The ontogeny of bumblebee flight trajectories: From naive explorers to experienced foragers (2013) Plos One, 8
  • Polster, J., Petrasch, J., Menzel, R., Landgraf, T., (2018) Reconstructing the Visual Perception of Honey Bees in Complex 3-D Worlds
  • Riley, J.R., Greggers, U., Smith, A.D., Stach, S., Reynolds, D.R., Stollhoff, N., The automatic pilot of honeybees (2003) Proc. Biol. Sci., 270, pp. 2421-2424
  • Riley, J.R., Reynolds, D.R., Smith, A.D., Edwards, A.S., Osborne, J.L., Williams, I.H., Compensation for wind drift by bumble-bees (1999) Nature, 400, p. 126
  • Riley, J.R., Smith, A.D., Reynolds, D.R., Edwards, A.S., Osborne, J.L., Williams, I.H., Tracking bees with harmonic radar (1996) Nature, 379, pp. 29-30
  • Schiffner, I., Fuhrmann, P., Wiltschko, R., Homing flights of pigeons in the Frankfurt region: The effect of distance and local experience (2013) Anim. Behav., 86, pp. 291-307
  • Se, S., Lowe, D.G., Little, J.J., Vision-based global localization and mapping for mobile robots (2005) IEEE Trans. Robot., 21, pp. 364-375
  • Seelig, J.D., Jayaraman, V., Neural dynamics for landmark orientation and angular path integration (2015) Nature, 521, pp. 186-191
  • Strecha, C., Küng, O., Fua, P., (2012) Automatic Mapping from Ultra-Light UAV Imagery, , EuroCOW 2012. No. EPFL-CONF-175351
  • Stürzl, W., Boeddeker, N., Dittmar, L., Egelhaaf, M., Mimicking honeybee eyes with a 280 degrees field of view catadioptric imaging system (2010) Bioinspir. Biomim., 5
  • Tison, L., Hahn, M.L., Holtz, S., Rößner, A., Greggers, U., Bischoff, G., Honey bees’ behavior is impaired by chronic exposure to the neonicotinoid thiacloprid in the field (2016) Environ. Sci. Technol., 50, pp. 7218-7227
  • Valiquette, C.M., McNamara, T.P., Labrecque, J.S., Biased representations of the spatial structure of navigable environments (2007) Psychol. Res., 71, pp. 288-297
  • von Frisch, K., Lindauer, M., Himmel und erde in konkurrenz bei der orientierung der bienen (1954) Naturwissenschaften, 41, pp. 245-253
  • Wiener, J., Shettleworth, S., Bingman, V.P., Cheng, K., Healy, S., Jacobs, L.F., Animal navigation, a synthesis (2011) Animal Thinking: Contemporary Issues in Comparative Cognition. Strpngmann Forum Reports, pp. 51-78. , eds J. Menzel and J. Fischer (Cambridge, MA: MIT Press
  • Wiltschko, R., Schiffner, I., Sigmund, B., Homing flights of pigeons over familiar terrain (2007) Anim. Behav., 74, pp. 1229-1240
  • Wolf, S., McMahon, D.P., Lim, K.S., Pull, C.D., Clark, S.J., Paxton, R.J., So near and yet so far: Harmonic radar reveals reduced homing ability of Nosema infected honeybees (2014) Plos One, 9

Citas:

---------- APA ----------
Menzel, R., Tison, L., Fischer-Nakai, J., Cheeseman, J., Balbuena, M.S., Chen, X., Landgraf, T.,..., Greggers, U. (2019) . Guidance of navigating honeybees by learned elongated ground structures. Frontiers in Behavioral Neuroscience, 12.
http://dx.doi.org/10.3389/fnbeh.2018.00322
---------- CHICAGO ----------
Menzel, R., Tison, L., Fischer-Nakai, J., Cheeseman, J., Balbuena, M.S., Chen, X., et al. "Guidance of navigating honeybees by learned elongated ground structures" . Frontiers in Behavioral Neuroscience 12 (2019).
http://dx.doi.org/10.3389/fnbeh.2018.00322
---------- MLA ----------
Menzel, R., Tison, L., Fischer-Nakai, J., Cheeseman, J., Balbuena, M.S., Chen, X., et al. "Guidance of navigating honeybees by learned elongated ground structures" . Frontiers in Behavioral Neuroscience, vol. 12, 2019.
http://dx.doi.org/10.3389/fnbeh.2018.00322
---------- VANCOUVER ----------
Menzel, R., Tison, L., Fischer-Nakai, J., Cheeseman, J., Balbuena, M.S., Chen, X., et al. Guidance of navigating honeybees by learned elongated ground structures. Front. Behav. Neurosci. 2019;12.
http://dx.doi.org/10.3389/fnbeh.2018.00322