Honey bees navigate according to a map-like spatial memory

Abstract

By using harmonic radar, we report the complete flight paths of displaced bees. Test bees forage at a feeder or are recruited by a waggle dance indicating the feeder. The flights are recorded after the bees are captured when leaving the hive or the feeder and are released at an unexpected release site. A sequence of behavioral routines become apparent: (i) initial straight flights in which they fly the course that they were on when captured (foraging bees) or that they learned during dance communication (recruited bees); (ii) slow search flights with frequent changes of direction in which they attempt to "get their bearings"; and (iii) straight and rapid flights directed either to the hive or first to the feeding station and then to the hive. These straight homing flights start at locations all around the hive and at distances far out of the visual catchment area around the hive or the feeding station. Two essential criteria of a map-like spatial memory are met by these results: bees can set course at any arbitrary location in their familiar area, and they can choose between at least two goals. This finding suggests a rich, map-like organization of spatial memory in navigating honey bees.

Fig. 1.

Study site and three representative flight paths. (A) Layout of the experimental site during the first period. Locations: the hive (H), the feeders (F_s, stationary feeder; F_v, variable feeder), the tents (▵), and the radar station (Radar). The circle around the hive has a radius of 60 m (visual angle of 1°). The ground structures resulting from differently mown grass and from soil conditions can be seen in this satellite image. A prominent extended ground structure was the borderline between two fields of grassland mown at different times that stretched from south-southwest to north-northeast and ran through the southern group of tents and the hive location during the first study period. During the second study period, the hive, feeder, tents, and radar station were shifted by 50 m to the east with respect to this borderline. (B) The profile of the horizon as seen from the hive. The maximal elevation above normal is ≈4°, and the angular variance lies within 1.5° and thus cannot be seen by the bees (see the supporting information). (C–E) Three examples of flight paths [SF bees (C), VF bees (D), and R bees (E)] showing the three flight phases: vector flight (bold line in SF and R bees), search flight (dotted line), and homing flight (thin line). The stars mark the homing points at each of the three tracks. (The supporting information provides 39 flight paths from all test groups.)

Fig. 2.

Homing flights and homing points of the three test groups. (A–C) Shown are 35 examples of homing flights of SF bees (A), VF bees (B), and R bees (C) tested with the normal arrangement of the tents. The homing flight component of the full trace was detected by using the algorithm described in Materials and Methods. The bees in A and B were released at different sites around the hive, and those in C were released from three release sites in the southeastern to southern part of the study area. The final flight path of each bee is shown with a different line. Flight traces in A and B were recorded in the first study period, and those in C were recorded in the second study period. Because R bees performed very short search flights, and because they were released in the southeastern to southern sector close to the southern groups of tents, it is not surprising that their homing flights are close together. Notice that the borderline was located 50 m to the east as compared with the first study period, and bees did not follow the borderline when homing. (D–F) Localization of homing points for the three experimental groups: SF and VF bees, first study period, normal tent arrangement (D); SF bees, rotated tent arrangement, first study period (E); and R bees, second study period (F). In F, the stars mark the homing flights of R bees under sunny weather conditions, and the crosses indicate those under an overcast sky. The homing points were calculated by using the algorithm described in Materials and Methods. The test with the rotated tents (E) proves that landmarks on the ground are sufficient to allow homing. Notice that most homing points are within the visual range of the tents when the tents are arranged normally, but very few lie close to the tents when they are rotated, indicating that the tents play a role in localization. The results from R bees under an overcast sky show that homing does not require the sun compass.

Fig. 3.

Homing flights via the feeder. Ten SF bees (of 29 bees tested under similar conditions) performed their homing flights via the feeder. Flight paths 2 and 3 come from bees that were tested during the second study period; the other paths come from those tested during the first study period. Bees released at release site 2 are shown by flight paths 1–5, and those released at release site 3 are indicated by flight paths 6–10. The bee from flight path 4 landed at the feeder and flew to the hive after filling its crop. All bees were tested with the normal arrangement of tents under sunny weather conditions. Notice that the coordinates are centered to the hive in an attempt to represent the flight paths of both study periods in one figure.

Fig. 4.

A model of the vector map. During observatory flights (curved lines with arrows), bees establish multiple associations between landmarks and the respective return headings and distances to the hive (dotted lines A and F). In addition, SF bees learn the heading and distance between the hive (H) and the feeder (F_s) (double-headed arrow labeled trained vectors). After being released at the release site (R) and applying the information about heading and distance from the feeder to the hive stored in working memory, bees search for a while. When SF bees find themselves at a location () at which a particular heading and distance are retrieved (A), they may either follow this information and return to the hive or switch their motivation and aim for the feeder. In such a situation they retrieve the vector components (heading and distance) of the outbound route flight from the hive-feeder to the feeder (C), which leads them to a new location (NL), or they perform some form of large-scale vector integration that leads them along a novel route to the feeder (B). At the novel location NL they may apply the same vector integration (D) or reach another known place (LRP) from which they go through the same procedure, use the associated flight parameters (F) to fly back to the hive directly or perform vector integration (G). However, our data also are consistent with the possibility that bees establish during orientation flights a relational map-like memory. In that case, they would localize themselves according to local landmarks and views, and they would choose a flight vector to the localizations of the hive or the feeder.