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Original Research ARTICLE Provisionally accepted The full-text will be published soon. Notify me

Front. Behav. Neurosci. | doi: 10.3389/fnbeh.2018.00322

Honeybees are Guided by Learned Elongated Ground Structures

 Randolf Menzel1*,  Lea Tison1,  Johannes Fischer-Nakai2,  James Cheeseman3, Konstantin Lehmann4,  Maria S. Balbuena5, Xiuxian Chen4,  Tim Landgraf6, Julian Petrasch6 and Uwe Greggers4
  • 1Neurobiology Unit, Freie Universität Berlin, Germany
  • 2Institute for Bee Science, Goethe University Frankfurt am Main, Germany
  • 3School of Biological Sciences, Faculty of Science, University of Auckland, New Zealand
  • 4Fachbereich Biologie, Chemie, Pharmazie, Freie Universität Berlin, Germany
  • 5Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina
  • 6Fachbereich Mathematik und Informatik, Freie Universität Berlin, Germany

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.

Keywords: navigation,, sun compass, guiding landmarks, object recognition, ground structures, Compass alignment

Received: 27 Aug 2018; Accepted: 07 Dec 2018.

Edited by:

Martin Giurfa, UMR5169 Centre de Recherches sur la Cognition Animale (CRCA), France

Reviewed by:

Ryuichi Okada, Kobe University, Japan
Franck Ruffier, Aix-Marseille Université, France  

Copyright: © 2018 Menzel, Tison, Fischer-Nakai, Cheeseman, Lehmann, Balbuena, Chen, Landgraf, Petrasch and Greggers. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Randolf Menzel, Freie Universität Berlin, Neurobiology Unit, Berlin, D-14195, Germany,