Third European Congress on Social Insects
St. Petersburg, Russia, 22-27 August 2005
Abstract for Plenary Lecture
Odor and honey bee exploitation of food crops
Adrian M. Wenner1
1Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, Santa Barbara, California, USA, 93106. E-mail: email@example.com
Keywords: honeybees, odors, learning, recruitment, wind, pollination
In 330 BC, Aristotle wrote (in part): “for instance, bees and [ants] detect [food] at a distance, and they do so recognizing it by smell.” Recent studies confirm that honeybees (Apis mellifera) are what some scientists view as the “ultimate generalist forager” (polylectic, not oligolectic). That is, no one seems to have yet found a “natural attractant” for honeybees, although some apparent exceptions exist. At times, searching bees will investigate the odor of honey and of wax. During swarm relocation, scout bees will orient toward Nasanov gland emissions. Drones in flight will fly toward airborne objects and attempt to mate with any object that has queen odor.
Flower scents, with their pleasant odors (pleasant to us, that is) have long been considered to attract “scout” bees. However, attempts to use such odors, their constituent chemicals, or Nasanov gland compounds to entice bees to pollinate crops have not proven successful.
To our senses, flower odors seem simple (e.g., rose, citrus, jasmine), but an analysis of such perfumes reveals that an entire suite of chemicals emanates from such blossoms. Some specific chemicals (e.g., citronella) occur across different flower species, but no pattern has yet been found to exist. We encounter, instead, a remarkable diversity of chemical combinations in the scents of various flowers.
Besides the fact that blossoms in a single flower species likely have a complex combination of odors, we who experiment must contend with the fact that each specific locality in nature also has a suite of odors that can define that locality. Consider, for example, any particular site in an open field. Weeds at that site may differ from an apparently similar site nearby. Establishing a feeding station can involve trampling on grass or weeds and contribute to the specific suite of odors at that site. Also, molecules from some odor source upwind can drift down to the station and cling to the body hairs of foragers. Although we human beings may not smell distinctive odors in the area, we have little evidence about which and how many odors honeybees might perceive. We can only determine that by experimentation.
Hypothesis: Bees rely on a suite of odors, as well as on visual and other cues, but do not necessarily rely on a single chemical at any one time.
Learning (conditioned response) in honeybees has not received the attention it should have received this past half century. Consider two comments that von Frisch published in 1950, statements that deserved more consideration back then (only slightly paraphrased here): A) When the feeding dishes became empty, only from time to time would one of [the foragers] fly out to the feeding place to see if anything was to be had. B) If we now refilled the dish at the more distant site, then the first gatherers to return with full stomachs aroused chiefly bees from the group that had previously visited the distant feeding place. But when we offered sugar water at the nearer site, then the [returning foragers] aroused mostly bees that had previously been feeding there.”
In the 1960s we obtained experimental results similar to those von Frisch had published but noticed that his results could occur even when returning successful bees did not dance. Today many of us would recognize that situation as an example of learning (conditioned response) behavior. Experienced foragers do investigate known nectar or pollen sources after they cease to yield a reward. When reward again becomes available, those investigating foragers feed and return to their colony. They carry odors on their bodies of the food and of the specific locality they frequented. Idled experienced foragers in the colony recognize from that particular set of odors that food is once again available. They then fly out to sites where they had previously had success. An exponential buildup of experienced foragers at profitable food sources thus occurs at similar sites in the entire region. We termed this type of recruitment, “communication by means of conditioned response.” To test that behavior, we let the dishes remain empty and later merely injected the training odor into the hive; experienced bees then soon arrived at the empty dishes on the basis of an odor cue alone.
Hypothesis: Recruitment of experienced bees each day can be explained by conditioned response, a recruitment to wherever the odor of similar food sources exists in the region.
One must therefore distinguish between the behavior of experienced foragers and newly recruited bees. Experienced foragers, upon perceiving a familiar odor, fly immediately out to previously yielding sources. By contrast, newly recruited bees receive a “reward” from a waggle dancer, obtain an impression of a suite of odors (of food and of locality) from that successful forager, and then instantly learn (become conditioned) to search for the same food source. On that point, von Frisch wrote in 1937, “the [recruited] bees first seek in the neighborhood, and then go farther away, and finally search the whole flying district.”
Consider an experiment with a constant number of marked foragers that make round trips between the feeding station and their colony. One can then continually capture and tally all unmarked bees as they arrive at the feeding station that has scented food. Each day experienced foragers will build up exponentially after initial provision of food. Recruits, by contrast, will not begin to arrive in numbers until an hour after regular foragers begin their trips. The increase in number of recruits captured per 15 minutes will be linear, not exponential, during a several hour experiment. If one repeats the experiment and then switches to unscented food half way through a preset time period, recruits will suddenly cease to arrive. That type of result matches what von Frisch wrote in 1937: “I succeeded with all kinds of flowers with the exception of flowers without any scent. When the collecting bee alights on the scented flowers to suck up the food, the scent of the flower is taken up by its body-surface and hairs, and when it dances after homing the interested bees perceive the specific scent on its body and know what kind of scent must be sought”
Hypothesis: Without odor, recruited bees cannot find a food source.
It is difficult to conduct completely odor-free experiments, since foraging bees function essentially as “flying dust mops” (Jerry Bromenshenk’s term). In normal circumstances, not only do they bring back to their colony odor of the food source but also the odor of the specific locality in which they forage. Bromenshenk’s experiments have revealed that bees can perceive molecular concentrations in parts per billion or parts per trillion.
Winds complicate the study of recruitment to food sources, a fact little appreciated until recently. Odor molecules can only travel downwind; hence, recruitment of bees to food sources located any great distance downwind from a colony becomes difficult. On the other hand, in most places wind directions shift daily and also shift from day to day as weather fronts pass through an area. In those cases, foraging can occur in all directions from a colony. In other places, wind can have a relatively constant direction during a season, and foraging occurs primarily in one direction.
From all of the above, it would appear that we might be on the verge of a breakthrough for a new era in studies of pollination. Anyone who has attempted to train bees to an artificial feeding station must have at times encountered difficulty. For instance, during a major nectar flow the odor of that incoming nectar accumulates in the colony. If one then attempts to train bees to a feeding station, the odor of the prevailing nectar flow overrides whatever small amount of odor one uses in sugar solution at a test feeding station.
In the 1930s and early 1940s, Gubin, Romashov, Kapustin, and Gataulin in Russia and von Frisch in Germany reported some success in “scent directing bees” to get them to forage on particular crops. Although some questions have been raised as to whether they really had achieved success, our own results suggest that a full application of current knowledge about odor, conditioned response, how to saturate colonies with target odor, and the importance of wind direction could well lead to important practical application.
Wenner, A.M. [with K. von Frisch]. 1993 . The language of bees. Bee World. 74:90-98. (Science Round-Up: The Language of Bees)
Wenner, A.M. 1998. Odors, wind and colony foraging – Part II of three parts: The role of wind direction. Am. Bee J. 138:807-810. (Odors, Wind and Colony Foraging (2 of 3): The Role of Wind Direction)
Wenner, A.M., D.E. Meade, and L.J. Friesen. 1991. Recruitment, search behavior, and flight ranges of honey bees. Amer. Zool. 31:768-782. (Recruitment, Search Behavior, and Flight Ranges of Honey Bees)
See also: (Adrian Wenner bio page)