Social learning of floral odours inside the honeybee hive

Abstract

A honeybee hive serves as an information centre in which communication among bees allows the colony to exploit the most profitable resources in a continuously changing environment. The best-studied communication behaviour in this context is the waggle dance performed by returning foragers, which encodes information about the distance and direction to the food source. It has been suggested that another information cue, floral scents transferred within the hive, is also important for recruitment to food sources, as bee recruits are more strongly attracted to odours previously brought back by foragers in both honeybees and bumble-bees. These observations suggested that honeybees learn the odour from successful foragers before leaving the hive. However, this has never been shown directly and the mechanisms and properties of the learning process remain obscure. We tested the learning and memory of recruited bees in the laboratory using the proboscis extension response (PER) paradigm, and show that recruits indeed learn the nectar odours brought back by foragers by associative learning and retrieve this memory in the PER paradigm. The associative nature of this learning reveals that information was gained during mouth-to-mouth contacts among bees (trophallaxis). Results further suggest that the information is transferred to long-term memory. Associative learning of food odours in a social context may help recruits to find a particular food source faster.

Figure 1

Percentage of bees that extended the proboscis on the first presentation of the odour. (a) Responses from the experimental hive (EH) during part 1. (b) Its corresponding odour condition: linalool in solution and phenylacetaldehyde in the EH during days 12, 13 and 14; unscented solution and phenylacetaldehyde in the EH between 15 and 18 days. (c) Responses from the control hive (CH) during part 1. (d) Responses from the EH during part 2. (e) Its corresponding odour condition: 2-nonanone in solution and linalool in the EH during days 38, 39 and 40, unscented solution and linalool in the EH between 41 and 44 days. (f) Responses from the CH during part 2. Responses for solution odour (grey), hive odour (white) and for both odours (black) for the EH and the CH. The CH was untreated in both situations. Asterisks indicate statistical differences (G_adj-test, *p<0.05, n.s., not significant; see §3 for details). Number of tested bees above bars.

Figure 2

Percentage of bees that extended the proboscis during a given trial. (a) Acquisition of bees from the experimental hive (EH) and control hive (CH) during the course of the differential PER conditioning. LIO was the CS+ and PHE was the CS−. (b) For conditioning with NON as CS+ and LIO as CS−.