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.

Odour aversion after olfactory conditioning of the sting extension reflex in honeybees

“…In this case, harnessed bees could not have learned to approach the odour during conditioning, thus showing that transfer between situations did indeed exist. The possible natural function of this transfer ability may be related to the observation that bees do indeed learn to associate odours and nectar reward within the hive during trophallaxis with returning foragers (Farina et al, 2005;Gil and De Marco, 2005), and subsequently choose the odour learnt within the hive in a foraging context (von Frisch, 1946;Arenas et al, 2007). Most importantly, these experiments also showed that after the formation of an odour-sucrose association, the learnt odour had acquired a positive/attractive nature for the animal.…”

Olfactory memory established during trophallaxis affects food search behaviour in ants

“…The acquisition of associative memories through a social interaction has already been shown or suggested in other social insects [honeybees (Farina et al, 2005;Farina et al, 2007;Gil and De Marco, 2005;Grüter et al, 2006); stingless bees (McCabe and Farina, 2009)], but its functional value in the context of food searching has not been proved before. In bees, the memories established during trophallaxis have been evaluated through a classical paradigm based on the proboscis extension reflex (PER) (Takeda, 1961;Bitterman et al, 1983).…”

“…In the last few years, many learning-related behaviours have been studied in the context of trophallactic interaction, particularly in bees (Farina et al, 2005;Farina et al, 2007;Gil and De Marco, 2005;Martinez and Farina, 2008). The acquisition of these memories is considered as social learning, defined as individual learning that takes place in a social context (Heyes, 1993;Brown and Laland, 2003;Leadbeater and Chittka, 2007).…”

Experimental identification of social learning in wild animals

“…We cannot fully review the many published studies here or in Table 1 but do point to experiments that illustrate a variety of valuable approaches to field sociallearning experiments. For example, demonstrators can be created by feeding them scented foods (Farina, Grüter, & Díaz, 2005) or training them to particular locations (Gould, 1975b). Social cues such as the waggle dance can be modified or eliminated in many ways-for example, by manipulations of the optical or light environment (Esch, Zhang, Srinivasan, & Tautz, 2001;Sherman & Visscher, 2002).…”