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Honeybees Learn Landscape Features during Exploratory Orientation Flights

2016; Elsevier BV; Volume: 26; Issue: 20 Linguagem: Inglês

10.1016/j.cub.2016.08.013

1879-0445

Jacqueline Degen, Andreas Kirbach, Lutz Reiter, Konstantin Lehmann, Philipp Norton, Mona Storms, Miriam Koblofsky, Sarah Winter, Petya Georgieva, Hai Nguyen, Hayfe Chamkhi, Hanno Gerd Meyer, P. K. Singh, Gisela Manz, Uwe Greggers, Randolf Menzel,

Insect and Arachnid Ecology and Behavior

Exploration is an elementary and fundamental form of learning about the structure of the world [1Tolman E.C. Cognitive maps in rats and men.Psychol. Rev. 1948; 55: 189-208Crossref PubMed Scopus (3663) Google Scholar, 2Birke L.I.A. Archer J. Some issues and problems in the study of animal exploration.in: Archer J. Birke L.I.A. Exploration in Animals and Humans. Van Nostrand Reinhold, 1983: 1-21Google Scholar, 3Renner M.J. Learning during exploration: the role of behavioral topography during exploration in determining subsequent adaptive behavior in the Sprague-Dawley rat (Rattus norvegicus).Int. J. Comp. Psychol. 1988; 2: 43-55Google Scholar]. Little is known about what exactly is learned when an animal seeks to become familiar with the environment. Navigating animals explore the environment for safe return to an important place (e.g., a nest site) and to travel between places [4Wiener J. Shettleworth S. Bingman V.P. Cheng K. Healy S. Jacobs L.F. Jeffrey K.J. Mallot H.A. Menzel R. Newcombe N.S. Animal navigation, a synthesis.in: Menzel R. Fischer J. Animal Thinking: Contemporary Issues in Comparative Cognition. MIT Press, 2011: 51-78Crossref Google Scholar]. Flying central-place foragers like honeybees (Apis mellifera) extend their exploration into distances from which the features of the nest cannot be directly perceived [5Lindauer M. Ein Beitrag zur Frage der Arbeitsteilung im Bienenstaat.Z. Vgl. Physiol. 1952; 34: 299-345Crossref Scopus (320) Google Scholar, 6Becker L. Untersuchungen über das Heimfindevermögen der Bienen.Z. Vgl. Physiol. 1958; 41: 1-25Google Scholar, 7von Frisch K. The Dance Language and Orientation of Bees. Harvard University Press, 1967Google Scholar, 8Vollbehr J. Zur Orientierung junger Honigbienen bei ihrem 1.Orientierungsflug. Zool. Jb. Physiol. 1975; 79: 33-69Google Scholar, 9Winston M.L. The Biology of the Honey Bee. Harvard University Press, 1987Google Scholar, 10Capaldi E.A. Smith A.D. Osborne J.L. Fahrbach S.E. Farris S.M. Reynolds D.R. Edwards A.S. Martin A. Robinson G.E. Poppy G.M. Riley J.R. Ontogeny of orientation flight in the honeybee revealed by harmonic radar.Nature. 2000; 403: 537-540Crossref PubMed Scopus (248) Google Scholar]. Bees perform short-range and long-range orientations flights. Short-range flights are performed in the immediate surroundings of the hive and occur more frequently under unfavorable weather conditions, whereas long-range flights lead the bees into different sectors of the surrounding environment [11Degen J. Kirbach A. Reiter L. Lehmann K. Norton P. Storms M. Koblofsky M. Winter S. Georgieva P.B. Nguyen H. et al.Exploratory behaviour of honeybees during orientation flights.Anim. Behav. 2015; 102: 45-57Crossref Scopus (61) Google Scholar]. Applying harmonic radar technology for flight tracking, we address the question of whether bees learn landscape features during their first short-range or long-range orientation flight. The homing flights of single bees were compared after they were displaced to areas explored or not explored during the orientation flight. Bees learn the landscape features during the first orientation flight since they returned faster and along straighter flights from explored areas as compared to unexplored areas. We excluded a range of possible factors that might have guided bees back to the hive based on egocentric navigation strategies (path integration, beacon orientation, and pattern matching of the skyline). We conclude that bees localize themselves according to learned ground structures and their spatial relations to the hive.