Honeybee navigation: critically examining the role of the polarization compass

Although it is widely accepted that honeybees use the polarized-light pattern of the sky as a compass for navigation, there is little direct evidence that this information is actually sensed during flight. Here, we ask whether flying bees can obtain compass cues derived purely from polarized light, and communicate this information to their nest-mates through the ‘waggle dance’. Bees, from an observation hive with vertically oriented honeycombs, were trained to fly to a food source at the end of a tunnel, which provided overhead illumination that was polarized either parallel to the axis of the tunnel, or perpendicular to it. When the illumination was transversely polarized, bees danced in a predominantly vertical direction with waggles occurring equally frequently in the upward or the downward direction. They were thus using the polarized-light information to signal the two possible directions in which they could have flown in natural outdoor flight: either directly towards the sun, or directly away from it. When the illumination was axially polarized, the bees danced in a predominantly horizontal direction with waggles directed either to the left or the right, indicating that they could have flown in an azimuthal direction that was 90° to the right or to the left of the sun, respectively. When the first half of the tunnel provided axial illumination and the second half transverse illumination, bees danced along all of the four principal diagonal directions, which represent four equally likely locations of the food source based on the polarized-light information that they had acquired during their journey. We conclude that flying bees are capable of obtaining and signalling compass information that is derived purely from polarized light. Furthermore, they deal with the directional ambiguity that is inherent in polarized light by signalling all of the possible locations of the food source in their dances, thus maximizing the chances of recruitment to it.

[1]  Rüdiger Wehner,et al.  E-Vector orientation in bees , 1978, Journal of comparative physiology.

[2]  G. D. Bernard,et al.  Twisted and non-twisted rhabdoms and their significance for polarization detection in the bee , 1975, Journal of comparative physiology.

[3]  M. Lindauer.  Communication Among Social Bees , 1961 .

[4]  Thomas Labhart,et al.  Specialized photoreceptors at the dorsal rim of the honeybee's compound eye: Polarizational and angular sensitivity , 1980, Journal of comparative physiology.

[5]  H. Heran,et al.  Beobachtungen über die Entfernungsmeldung der Sammelbienen , 1952, Zeitschrift für vergleichende Physiologie.

[6]  M V Srinivasan,et al.  Honeybee navigation: nature and calibration of the "odometer". , 2000, Science.

[7]  M. Srinivasan,et al.  Honeybee navigation: distance estimation in the third dimension , 2007, Journal of Experimental Biology.

[8]  Rüdiger Wehner,et al.  The POL area of the honey bee's eye: behavioural evidence , 1985 .

[9]  R. Wehner.  The Hymenopteran Skylight Compass: Matched Filtering and Parallel Coding , 1989 .

[10]  N. Strausfeld,et al.  Evolution, discovery, and interpretations of arthropod mushroom bodies. , 1998, Learning & memory.

[11]  Stanley Heinze.  Polarization Vision , 2014, Encyclopedia of Computational Neuroscience.

[12]  Mandyam V. Srinivasan,et al.  Honeybee navigation: properties of the visually driven `odometer' , 2003, Journal of Experimental Biology.

[13]  Bernhard Ronacher,et al.  The polarization compass dominates over idiothetic cues in path integration of desert ants , 2012, Journal of Experimental Biology.

[14]  K. Frisch.  The dance language and orientation of bees , 1967 .

[15]  R. Wehner,et al.  Skylight polarization as perceived by desert ants and measured by video polarimetry , 1999, Journal of Comparative Physiology A.

[16]  Rüdiger Wehner,et al.  Polarization vision in bees , 1986, Nature.

[17]  N. Strausfeld,et al.  Mushroom bodies of the cockroach: Their participation in place memory , 1998, The Journal of comparative neurology.

[18]  R. Morse.  The Dance Language and Orientation of Bees , 1994 .

[19]  M V Srinivasan,et al.  Honeybee navigation: following routes using polarized-light cues , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[20]  M. Sanders.  Handbook of Sensory Physiology , 1975 .

[21]  A. Rady.  Effect of change in environmental temperature on antioxidant enzyme activities and lipid peroxidation in red blood cells of carp , 1993 .

[22]  Georg Birukow,et al.  Menotaxis im polarisierten Licht beiGeotrupes silvaticus Panz , 1953, Die Naturwissenschaften.

[23]  Herbert Heran,et al.  Ein Beitrag zur Frage nach der Wahrnehmungsgrundlage der Entfernungsweisung der Bienen (Apis mellifica L.) , 2004, Zeitschrift für vergleichende Physiologie.

[24]  K. Frisch,et al.  Die Polarisation des Himmelslichtes als orientierender Faktor bei den Tänzen der Bienen , 1949, Experientia.

[25]  N. Strausfeld,et al.  Mushroom bodies of the cockroach: Activity and identities of neurons recorded in freely moving animals , 1998, The Journal of comparative neurology.

[26]  Una F. Jacobs-Jessen.  Zur Orientierung der Hummeln und einiger anderer Hymenopteren , 1959, Zeitschrift für vergleichende Physiologie.

[27]  Zhang,et al.  Visually mediated odometry in honeybees , 1997, The Journal of experimental biology.

[28]  Randolf Menzel,et al.  Encoding spatial information in the waggle dance , 2005, Journal of Experimental Biology.

[29]  William F. Towne,et al.  The connection between landscapes and the solar ephemeris in honeybees , 2008, Journal of Experimental Biology.

[30]  R. Wehner,et al.  The bee's map of the e-vector pattern in the sky. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[31]  J. L. Gould,et al.  Skylight Polarization patterns and Animal Orientation , 1982 .

[32]  G. Hoffmann.  Homing by Systematic Search , 1984 .

[33]  Fred C. Dyer,et al.  Sun-Compass Learning in Insects , 1996 .

[34]  T. Labhart,et al.  Neural mechanisms in insect navigation: polarization compass and odometer , 2002, Current Opinion in Neurobiology.

[35]  Shaowu Zhang,et al.  Honeybee dances communicate distances measured by optic flow , 2001, Nature.

[36]  B. Heller.  Circular Statistics in Biology, Edward Batschelet. Academic Press, London & New York (1981), 371, Price $69.50 , 1983 .

[37]  Samuel Rossel,et al.  Navigation by bees using polarized skylight , 1993 .

[38]  William F. Towne,et al.  Honeybees can learn the relationship between the solar ephemeris and a newly-experienced landscape , 2008, Journal of Experimental Biology.

[39]  M. I. Mote,et al.  Polarization sensitivity , 2004, Journal of comparative physiology.