Honey bees flexibly use two navigational memories when updating dance distance information

ABSTRACT Honey bees can communicate navigational information which makes them unique amongst all prominent insect navigators. Returning foragers recruit nest mates to a food source by communicating flight distance and direction using a small scale walking pattern: the waggle dance. It is still unclear how bees transpose flight information to generate corresponding dance information. In single feeder shift experiments, we monitored for the first time how individual bees update dance duration after a shift of feeder distance. Interestingly, the majority of bees (86%) needed two or more foraging trips to update dance duration. This finding demonstrates that transposing flight navigation information to dance information is not a reflexive behavior. Furthermore, many bees showed intermediate dance durations during the update process, indicating that honey bees highly likely use two memories: (i) a recently acquired navigation experience and (ii) a previously stored flight experience. Double-shift experiments, in which the feeder was moved forward and backward, created an experimental condition in which honey bee foragers did not update dance duration; suggesting the involvement of more complex memory processes. Our behavioral paradigm allows the dissociation of foraging and dance activity and opens the possibility of studying the molecular and neural processes underlying the waggle dance behavior. Summary: Individual honey bees flexibly use recently acquired navigation experience and previously stored navigation information to generate waggle dance duration for a novel feeder distance.

[1]  M V Srinivasan,et al.  Two odometers in honeybees? , 2008, Journal of Experimental Biology.

[2]  Ken Cheng,et al.  Experimental ethology of learning in desert ants: Becoming expert navigators , 2019, Behavioural Processes.

[3]  Ken Cheng,et al.  Skyline retention and retroactive interference in the navigating Australian desert ant, Melophorus bagoti , 2017, Journal of Comparative Physiology A.

[4]  K. Cheng,et al.  Honeybees (Apis mellifera) holding on to memories: response competition causes retroactive interference effects , 2006, Animal Cognition.

[5]  David R. Anderson,et al.  Understanding AIC and BIC in Model Selection , 2004 .

[6]  F. Dyer The biology of the dance language. , 2002, Annual review of entomology.

[7]  M. Srinivasan,et al.  Honeybee Odometry: Performance in Varying Natural Terrain , 2004, PLoS biology.

[8]  Fred C. Dyer,et al.  Memory and sun compensation by honey bees , 1987, Journal of Comparative Physiology A.

[9]  B. Webb,et al.  An Anatomically Constrained Model for Path Integration in the Bee Brain , 2017, Current Biology.

[10]  R. Wehner,et al.  Visual navigation in insects: coupling of egocentric and geocentric information , 1996, The Journal of experimental biology.

[11]  Michael H. Dickinson,et al.  Sun Navigation Requires Compass Neurons in Drosophila , 2018, Current Biology.

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

[13]  R. Wehner Desert ant navigation: how miniature brains solve complex tasks , 2003, Journal of Comparative Physiology A.

[14]  G. Robinson,et al.  Distance‐responsive genes found in dancing honey bees , 2010, Genes, brain, and behavior.

[15]  T. Collett,et al.  Spatial Memory in Insect Navigation , 2013, Current Biology.

[16]  F. Mery,et al.  A natural genetic polymorphism affects retroactive interference in Drosophila melanogaster , 2011, Proceedings of the Royal Society B: Biological Sciences.

[17]  M. Dickinson,et al.  Flying Drosophila Orient to Sky Polarization , 2012, Current Biology.

[18]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[19]  J. Armstrong,et al.  Functional dissection of the neural substrates for gravitaxic maze behavior in Drosophila melanogaster , 2007, The Journal of comparative neurology.

[20]  Steven M. Reppert,et al.  Navigational mechanisms of migrating monarch butterflies , 2010, Trends in Neurosciences.

[21]  Dance Type and Flight Parameters Are Associated with Different Mushroom Body Neural Activities in Worker Honeybee Brains , 2011, PloS one.

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

[23]  Randolf Menzel,et al.  Navigation and Communication in Honey Bees , 2012 .

[24]  R. Menzel,et al.  Exploratory behaviour of honeybees during orientation flights , 2015, Animal Behaviour.

[25]  J. L. Gould,et al.  Honey Bee Orientation: A Backup System for Cloudy Days , 1981, Science.

[26]  D. Gilley,et al.  Hydrocarbons Emitted by Waggle-Dancing Honey Bees Increase Forager Recruitment by Stimulating Dancing , 2014, PloS one.

[27]  Stanley Heinze,et al.  Maplike Representation of Celestial E-Vector Orientations in the Brain of an Insect , 2007, Science.

[28]  William F. Towne,et al.  Honeybees use the skyline in orientation , 2017, Journal of Experimental Biology.

[29]  D. Ventura,et al.  Effect of the Decrease in Luminance Noise Range on Color Discrimination of Dichromats and Trichromats , 2018, Front. Behav. Neurosci..

[30]  F. Dyer,et al.  Deciding when to explore and when to persist: a comparison of honeybees and bumblebees in their response to downshifts in reward , 2011, Behavioral Ecology and Sociobiology.

[31]  Gene E. Robinson,et al.  Central Projections of Sensory Systems Involved in Honey Bee Dance Language Communication , 2007, Brain, Behavior and Evolution.

[32]  R. Perrone,et al.  Status-Dependent Vasotocin Modulation of Dominance and Subordination in the Weakly Electric Fish Gymnotus omarorum , 2018, Front. Behav. Neurosci..

[33]  Francis L. W. Ratnieks,et al.  Intra-dance variation among waggle runs and the design of efficient protocols for honey bee dance decoding , 2012, Biology Open.

[34]  S. Morreale,et al.  Changepoint analysis: a new approach for revealing animal movements and behaviors from satellite telemetry data , 2015 .

[35]  Uwe Homberg,et al.  Sky Compass Orientation in Desert Locusts—Evidence from Field and Laboratory Studies , 2015, Front. Behav. Neurosci..

[36]  S. Al-Moghrabi,et al.  Inorganic carbon uptake for photosynthesis by the symbiotic coral-dinoflagellate association II. Mechanisms for bicarbonate uptake , 1996 .

[37]  R. Menzel,et al.  A Common Frame of Reference for Learned and Communicated Vectors in Honeybee Navigation , 2011, Current Biology.

[38]  T. Hothorn,et al.  Simultaneous Inference in General Parametric Models , 2008, Biometrical journal. Biometrische Zeitschrift.

[39]  John A. Wolf,et al.  Neural Substrate Expansion for the Restoration of Brain Function , 2016, Front. Syst. Neurosci..

[40]  R. Menzel,et al.  Exploratory behavior of re-orienting foragers differs from other flight patterns of honeybees , 2018, PloS one.

[41]  Mandyam V. Srinivasan Going with the flow: a brief history of the study of the honeybee’s navigational ‘odometer’ , 2014, Journal of Comparative Physiology A.

[42]  Matthew Collett,et al.  Path integration in insects , 2000, Current Opinion in Neurobiology.

[43]  Allen Cheung,et al.  Principles of Insect Path Integration , 2018, Current Biology.

[44]  Aaron S. Heller,et al.  Cortical-Subcortical Interactions in Depression: From Animal Models to Human Psychopathology , 2016, Front. Syst. Neurosci..

[45]  M. Lindauer,et al.  Dauertänze im Bienenstock und ihre Beziehung zur Sonnenbahn , 2004, Naturwissenschaften.

[46]  Jutta Kretzberg,et al.  Single and Multiple Change Point Detection in Spike Trains: Comparison of Different CUSUM Methods , 2016, Front. Syst. Neurosci..

[47]  Steven M. Reppert,et al.  Connecting the Navigational Clock to Sun Compass Input in Monarch Butterfly Brain , 2005, Neuron.