When do honey bees use snapshots during navigation?

1. Departing Wasp Returning Wasp Niko Tinbergen (1938) When do honey bees use snapshots during navigation? • Bees and wasps learn information about visual landmarks near the goal • Edge orientation (Srinivasan et al., 1994) • Color (von Frisch, 1967; Cheng et al., 1986) • Size (Cartwright & Collett, 1979; Ronacher, 1998) • Spatial relationships among multiple landmarks (Cartwright & Collett, 1983) • How is this information subsequently used over successive visits? • Snapshot template matching (Cartwright & Collett, 1983) By Frank Bartlett

2. After Cartwright & Collett, 1983 Upon return the bee steers flight by sequentially matching her memory to the environment View of landmarks is memorized from the goal What is snapshot navigation?

3. Single Landmark 3 equidistant Landmarks Training Training Landmark Goal Goal From Cartwright & Collett, 1983 Landmarks Distance from landmark Experiments revealing the contents of snapshot memories -- When a single landmark is present bees rely on retinal image size. -- When multiple landmarks are available bees rely on the inter-landmark angles (or the spaces between landmarks)

4. Testing the snapshot hypothesis in a small scale arena environment • The snapshot hypothesis makes accurate predictions about where insects should spend their time searching for the goal. • Can we replicate these findings? • The hypothesis also generates predictions of flight paths to the goal from more distant locations. • Do steering commands generated by snapshot matching predict honey bee flight behavior while en-route to a familiar goal? • This has not been tested explicitly.

5. Methods Training: bees visit an initial landmark configuration (60+ visits) Testing: track with original configuration and other landmark manipulations The camera records bee position and body axis orientation at 60 Hz.

6. Replication of Cartwright & Collett (1983) 2 x Training Search distributions -- When a single landmark is present bees rely on retinal image size. -- When multiple landmarks are available bees rely on the inter-landmark angles -- These results are consistent with previous studies

7. Bee Flights Model F E Flight paths to the goal location The model predictions were generated in Matlab based on the algorithm provided by Cartwright & Collett (1983) Bees appear to be attracted to the nearest landmark and use it as a beacon even over very short distances

8. Conclusions • Search at the goal • Consistent with previous findings • Steering from more remote locations using template matching • Bee flights not consistent with model predictions • Strong role of beacons • Consistent with other results (Fry & Wehner, 2005; Collett & Baron, 1994) but extended to shorter distances and more complex arrays • Beacon selection probably driven by visual salience

9. NSF IGERT Fred Dyer Steven Fry Mike Mack Chris Speilburg Yoav Littman Jenny Jones Lora Bramlett Kourtney Trudgen Lauren Davenport Acknowledgments

10. Niko Tinbergen (1938) Short range visual navigation in flying hymenopterans • Bees and wasp learn information about visual landmarks near the goal • Edge orientation (Srinivasan et al.; 1994) • Color (von Frisch, 1967; Cheng et al., 1986) • Size (Cartwright & Collett, 1979; Ronacher, 1998) • Spatial relationships among multiple landmarks (Cartwright & Collett; 1983) • How is this information represented and subsequently used over successive visits? • Snapshot template matching (Cartrwright & Collett; 1983)

11. First Visit Tenth Visit From Lehrer, 1993 How is this information learned?The turn-back-and-look --Motion parallax cues allow bees to distinguish nearby landmarks from distant landmarks (Lehrer, 1993) --Believed to aid in the selection and learning of the landmarks near a goal

12. After Cartwright & Collett, 1983 Bee sequentially matches her memory to the environment upon return View of landmarks is memorized from the goal What is snapshot navigation? -- Insect visual memory is thought to be comprised of a two dimensional “snapshot” that encodes the retinotopic sizes and positions of landmarks and the gaps between them.

13. F E Model predictions vs. Flight Behavior:pushed off course After their course is diverted by the novel landmark, bees again use the next nearest landmark as a beacon to guide flight.

14. Finding the match • Near the goal bees prefer to maintain a southern facing body axis • Snapshot is probably anchored to the retina (Collett & Baron, 1994) • Bees perform bouts of lateral flight during their return to the goal • Probably to help bring their memory into register with their current view (Collett & Reese, 1997)

15. F E Model predictions vs. flight Behavior:middle landmark removed

16. F E Model predictions vs. Flight Behavior:farthest landmark removed

17. F E Model predictions vs. Flight Behavior: removed nearest landmark

18. 2060 * 1830 * 1550 Fixed body axis and scanning flights Bees preferred a southern facing body axis orientation during their first pass through the goal region Bees rarely performed lateral scanning flights near the landmark. Circling flights were the norm.

19. Snapshot overview • Insects memorize a visual template or “snapshot” of landmarks they experience at important locations of their environment • The memory encodes the sizes and retinal locations of landmarks • Insects sequentially match this template to the environment upon return while maintaining consistent body alignment • Lateral scanning movement may aid the matching process

20. Snapshot overview • Insects memorize a visual template or “snapshot” of landmarks they experience at important locations of their environment • The memory encodes the sizes and retinal locations of landmarks • Insects sequentially match this template to the environment upon return while maintaining consistent body alignment • Lateral scanning movement may aid the matching process

21. Testing the snapshot hypothesis in a small scale arena environment • Honey bee flight behavior during other visual navigation experiments in our apparatus appeared inconsistent with snapshot guidance. • Investigated elements of snapshot navigation in a carefully controlled arena environment • Snapshot predictions of search behavior near the goal location (tested by Cartwright & Collett, 1979, 1982; Cheng, 1999) • Predictions of flights paths to the goal from distances of up to two meters (largely untested) • Consistent body axis orientation near the goal (Collett & Baron, 1994) • Lateral scanning flights near the goal (Collett & Rees, 1997)