Christoph Grüter

Social learning of floral odours inside the honeybee hive

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.

Honeybees learn floral odors while receiving nectar from foragers within the hive

Recent studies showed that nectar odors brought back by honeybee foragers can be learned associatively inside the hive. In the present study, we focused on the learning abilities of bees, which directly interact via trophallaxis with the incoming nectar foragers: the workers that perform nectar-receiving tasks inside the hive. Workers that have received food directly from foragers coming back from a feeder offering either unscented or scented sugar solution [phenylacetaldehyde (PHE) or nonanal diluted] were captured from two observational hives, and their olfactory memories were tested using the proboscis extension response paradigm. Bees that have received scented solution from incoming foragers showed significantly increased response frequencies for the corresponding solution odor in comparison with those that have received unscented solution. No differences in the response frequencies were found between food odors and colonies. The results indicate that first-order receivers learn via trophallaxis the association between the scent and the sugar solution transferred by incoming foragers. The implications of these results should be considered at three levels: the operational cohesion of bees involved in foraging-related tasks, the information propagation inside the hive related to the floral type exploited, and the putative effect of these memories on future preferences for resources.

Decision making in ant foragers (Lasius niger) facing conflicting private and social information

Foragers of many ant species use pheromone trails to guide nestmates to food sources. During foraging, individual workers can also learn the route to a food source. Foragers of the mass-recruiting ant Lasius niger use both pheromone trails and memory to locate a food source. As a result, an experienced forager can have a conflict between social information (trail pheromones) and private information (route memory) at trail bifurcations. We tested decision making in L. niger foragers facing such an informational conflict in situations where both the strength of the pheromone trail and the number of previous visits to the food source varied. Foragers quickly learned the branch at a T bifurcation that leads to a food source, with 74.6% choosing correctly after one previous visit and 95.3% after three visits. Pheromone trails had a weaker effect on choice behaviour of naïve ants, with only 61.6% and 70.2% choosing the branch that had been marked by one or 20 foragers versus an unmarked branch. When there was a conflict between private and social information, memory overrides pheromone after just one previous visit to a food source. Most ants, 82–100%, chose the branch where they had collected food during previous foraging trips, with the proportion depending on the number of previous trips (1 v. 3) but not on the strength of the pheromone trail (1 v. 20). In addition, the presence of a pheromone trail at one branch in a bifurcation had no effect on the time it took an experienced ant to choose the correct branch (the branch without pheromone). These results suggest that private information (navigational memory) dominates over social information (chemical tail) in orientation decisions during foraging activities in experienced L. niger foragers.

Informational conflicts created by the waggle dance

The honeybee (Apis mellifera) waggle dance is one of the most intriguing animal communication signals. A dancing bee communicates the location of a profitable food source and its odour. Followers may often experience situations in which dancers indicate an unfamiliar location but carry the scent of a flower species the followers experienced previously at different locations. Food scents often reactivate bees to resume food collection at previously visited food patches. This double function of the dance creates a conflict between the social vector information and the private navigational information. We investigated which kind of information followers with field experience use in this situation and found that followers usually ignored the spatial information encoded by the waggle dance even if they followed a dance thoroughly (five waggle runs or more). They relied on private information about food source locations instead (in 93% of all cases). Furthermore, foragers preferred to follow dancers carrying food odours they knew from previous field trips, independently of the spatial information encoded in the dance. Surprisingly, neither odour identity nor the location indicated by the dancer was an important factor for the reactivation success of a dance. Our results contrast with the assumption that (i) followers usually try to decode the vector information and (ii) dances indicating an unfamiliar location are of little interest to experienced foragers.

Insights from insects about adaptive social information use.

Copying others can greatly improve individual fitness and is fundamental for the organisation of societies. Yet in some situations it is better to ignore social information and either explore the world individually or use personal information obtained through prior experience. Insects provide excellent models to study the strategic use of social information, but insights from recent research have rarely been viewed in the light of social learning strategies. Here we discuss how insects tailor their reliance on social information to those circumstances for which it is most beneficial, and suggest that insects and vertebrates use similar information-use strategies. We highlight future research avenues, including the use of molecular tools to study the genetic and genomic basis of social information use.

A morphologically specialized soldier caste improves colony defense in a neotropical eusocial bee

Division of labor among workers is common in insect societies and is thought to be important in their ecological success. In most species, division of labor is based on age (temporal castes), but workers in some ants and termites show morphological specialization for particular tasks (physical castes). Large-headed soldier ants and termites are well-known examples of this specialization. However, until now there has been no equivalent example of physical worker subcastes in social bees or wasps. Here we provide evidence for a physical soldier subcaste in a bee. In the neotropical stingless bee Tetragonisca angustula, nest defense is performed by two groups of guards, one hovering near the nest entrance and the other standing on the wax entrance tube. We show that both types of guards are 30% heavier than foragers and of different shape; foragers have relatively larger heads, whereas guards have larger legs. Low variation within each subcaste results in negligible size overlap between guards and foragers, further indicating that they are distinct physical castes. In addition, workers that remove garbage from the nest are of intermediate size, suggesting that they might represent another unrecognized caste. Guards or soldiers are reared in low but sufficient numbers (1–2% of emerging workers), considering that <1% usually perform this task. When challenged by the obligate robber bee Lestrimelitta limao, an important natural enemy, larger workers were able to fight for longer before being defeated by the much larger robber. This discovery opens up opportunities for the comparative study of physical castes in social insects, including the question of why soldiers appear to be so much rarer in bees than in ants or termites.

Propagation of olfactory information within the honeybee hive

Transfer of information about food source characteristics within insect societies is essential to colony-foraging success. The food odor communicated within honeybee hives has been shown to be important for food source exploitation. When successful foragers return to the nest and transfer the collected nectar to hive mates through mouth-to-mouth contacts (trophallaxis), potential recruits receiving these samples learn the food odor by associative learning. The food then becomes rapidly distributed among colony members, which is mainly a consequence of the numerous trophallaxes between hive-mates of all ages during food processing. We tested whether the distribution of food among hive mates causes a propagation of olfactory information within the hive. Using the proboscis extension response paradigm, we show that large proportions of bees of the age groups representing the main worker castes, 4 to 9-day-old bees (nurse-aged bees), 12 to 16-day-old bees (food processor-aged bees), and actual foragers (about 17+ day old bees) associatively learn the food odor in the course of processing food that has been collected by only a few foragers. Results further suggest that the information is shared more or less equally between bees of the three age groups. This shows that olfactory information about the flower species exploited by foragers is distributed within the entire colony and is acquired by bees of all age groups, which may influence many behaviors inside and outside the hive.

Synergy between social and private information increases foraging efficiency in ants

Insect societies integrate many information sources to organize collective activities such as foraging. Many ants use trail pheromones to guide foragers to food sources, but foragers can also use memories to find familiar locations of stable food sources. Route memories are often more accurate than trail pheromones in guiding ants, and are often followed in preference to trail pheromones when the two conflict. Why then does the system expend effort in producing and acquiring seemingly redundant and low-quality information, such as trail pheromones, when route memory is available? Here we show that, in the ant Lasius niger, trail pheromones and route memory act synergistically during foraging; increasing walking speed and straightness by 25 and 30 per cent, respectively, and maintaining trail pheromone deposition, but only when used together. Our results demonstrate a previously undescribed major role of trail pheromones: to complement memory by allowing higher confidence in route memory. This highlights the importance of multiple interacting information sources in the efficient running of complex adaptive systems.

Trail Pheromones: An Integrative View of Their Role in Social Insect Colony Organization

Trail pheromones do more than simply guide social insect workers from point A to point B. Recent research has revealed additional ways in which they help to regulate colony foraging, often via positive and negative feedback processes that influence the exploitation of the different resources that a colony has knowledge of. Trail pheromones are often complementary or synergistic with other information sources, such as individual memory. Pheromone trails can be composed of two or more pheromones with different functions, and information may be embedded in the trail network geometry. These findings indicate remarkable sophistication in how trail pheromones are used to regulate colony-level behavior, and how trail pheromones are used and deployed at the individual level.

Ant foraging on complex trails: route learning and the role of trail pheromones in Lasius niger

SUMMARY Ants are central place foragers and use multiple information sources to navigate between the nest and feeding sites. Individual ants rapidly learn a route, and often prioritize memory over pheromone trails when tested on a simple trail with a single bifurcation. However, in nature, ants often forage at locations that are reached via more complex routes with multiple trail bifurcations. Such routes may be more difficult to learn, and thus ants would benefit from additional information. We hypothesized that trail pheromones play a more significant role in ant foraging on complex routes, either by assisting in navigation or route learning or both. We studied Lasius niger workers foraging on a doubly bifurcating trail with four end points. Route learning was slower and errors greater on alternating (e.g. left–right) versus repeating routes (e.g. left–left), with error rates of 32 and 3%, respectively. However, errors on alternating routes decreased by 30% when trail pheromone was present. Trail pheromones also aid route learning, leading to reduced errors in subsequent journeys without pheromone. If an experienced forager makes an error when returning to a food source, it reacts by increasing pheromone deposition on the return journey. In addition, high levels of trail pheromone suppress further pheromone deposition. This negative feedback mechanism may act to conserve pheromone or to regulate recruitment. Taken together, these results demonstrate further complexity and sophistication in the foraging system of ant colonies, especially in the role of trail pheromones and their relationship with learning and the use of private information (memory) in a complex environment.