AbstractThe behaviour of walking honeybees in small gradient odour fields was investigated by means of a simulation technique. The bee was kept in one place by a locomotion compensator (‘running sphere’). This compensator allowed for a precise reconstruction of the bee's actual locomotion on the sphere, and presented the bee with a stimulating odour whose concentration was controlled by feedback from the reconstructed locomotion. This rendered possible the application of well‐defined odour fields and revealed that: (1) honeybees are capable of finding odour sources in the absence of optical cues and with concentration gradients too small to allow tropotactic or klinotactic orientation; (2) bees are capable of memorizing odour concentrations with a high degree of accuracy; (3) this orientation system is based on a switching over from negative to positive anemotaxis at a ‘reference’ concentration; (4) this reference is a function of the odour concentration at which a sugar reward is given. The results do not support any hypothesis for an orientation system based on the detection and comparison of successive values of odour concentration. A hypothesis on the nature of the ‘reference value’ is discussed and supported b