In-hive learning of specific mimic odours as a tool to enhance honey bee foraging and pollination activities in pear and apple crops.

The areas devoted to agriculture that depend on pollinators have been sharply increased in the last decades with a concomitant growing global demand for pollination services. This forces to consider new strategies in pollinators' management to improve their efficiency. To promote a precision pollination towards a specific crop, we developed two simple synthetic odorant mixtures that honey bees generalized with their respective natural floral scents of the crop. We chose two commercial crops for fruit production that often coexist in agricultural settings, the apple (Malus domesticus) and the pear trees (Pyrus communis). Feeding colonies with sucrose solution scented with the apple mimic (AM) or the pear mimic (PM) odour enabled the establishment of olfactory memories that can bias bees towards the flowers of these trees. Encompassing different experimental approaches, our results support the offering of scented food to improve foraging and pollination activities of honey bees. The circulation of AM-scented sucrose solution inside the hive promoted higher colony activity, probably associated with greater activity of nectar foragers. The offering of PM-scented sucrose solution did not increase colony activity but led to greater pollen collection, which is consistent with pear flowers offering mainly pollen as resources for the bees. Results obtained from apple and pear crops suggest that the offering of AM- and PM-scented sucrose solution increased fruit yields. This preliminary study highlights the role of in-hive olfactory learning to bias foraging preferences within pome fruit crops.

Learning of a Mimic Odor within Beehives Improves Pollination Service Efficiency in a Commercial Crop.

The growing global demand for pollination services leads producers to consider new strategies in pollinator management to improve its efficiency in agroecosystems [1-3]. Central place foragers, like honeybees, learn floral cues not only in the field but also inside the nest, where resource cues introduced into the hive improve foraging by guiding bees toward the learned stimuli [4]. In this regard, attempts to condition bees with crop-odor-scented food produced ambiguous results and lacked yield measurements [5-7]. To deepen our understanding of the use of odors as part of a precision pollination strategy, we developed a simple synthetic odorant mixture that bees generalized with the natural floral scent of sunflower for hybrid seed production, an economically important and highly pollinator-dependent crop [8]. Encompassing different experimental approaches, our results show that feeding colonies food scented with the sunflower mimic (SM) odor enabled the establishment of olfactory memories that biased bees to the sunflower crop. The offering of a rewarded odor mimicking the sunflower floral fragrance promoted higher foraging activity, increased the proportion of dances advertising the target inflorescences and reduced delays in dance onset, positively affected the density of bees on the crop, and increased yields from 29% to 57% in different sunflower hybrids. This study highlights the role of olfactory learning within the social context of the hive to bias foraging preferences in a novel agricultural environment and suggest that improvements in the tested parameters were due to bees anticipated response to the sunflower scent.

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.