| Odors, Wind
and Colony Foraging Part I of Three Parts: The Need for Odor |
| by
ADRIAN M. WENNER 967 Garcia Road Santa Barbara, California 93103 (805) 963-8508 wenner@lifesci.ucsb.edu "One of my beekeeper friends...wrote to me that he obtained four unquestionable [bits of evidence for a 'language' among bees]. ...But I am convinced that my friend was misled by his desire, a very natural one, to see the experiment succeed." Maurice Maeterlinck - 1901 Steve Taber, in his three part series in The American Bee Journal (April, May, June issues) and in an earlier publication (Bogdany and Taber, 1979), held that: 1) a bee stimulated to leave the hive during the dance maneuver can later locate an unscented sugar solution in the field, and 2) searching bees can independently fly directly to a food source visited by foragers that regularly fly a considerable distance cross-wind to that source of food. Much evidence conflicts with those and other claims in the recent Taber series and in the original Bogdany and Taber study. In this series I will reveal how searching bees must rely on odor (Part I), clarify the importance of wind for success by searching bees (Part II), and provide new results in cases where crosswind recruitment failed even with odor provided (Part III). That third part will also outline simple experiments that anyone can conduct so that they can thereby independently judge for themselves the validity of diverse claims. Background - Centuries of Observation Beekeepers know that they can trust most of what they themselves observe and learn from their bees and their colonies. They realize that failure to attend to what one perceives can lead to colony loss. By contrast, articles or books about bees may contain statements that do not mesh with what beekeepers might observe about the actual behavior of bees or colonies. More puzzling, the books and articles they consult may omit information of vital importance to a beekeeper. To clarify that matter, consider the following quotations (full references in Wenner and Wells, 1990; Wenner, 1993): 330 B.C. Aristotle. "For all insects as a class, have, thanks to the species of odour correlated with nutrition, a keen olfactory sense of their proper food from a distance, even when they are very far away from it; such is the case with the bees." 1609 A.D. Charles Butler (author of a classic volume, The World of the Honeybee). "Their smelling is excellent, whereby, when they fly aloft in the air, they will quickly perceive anything under them that they like, as honey, or tar [for producing propolis], though it be covered; as soon as the honeydew is fallen, they presently [take wind of] it, though the oaks that [produce] it be afar off." 1924. Bruce Lineburg. "The theory of a scented trail [that recruited bees can exploit] is strengthened by the apparent elimination of other theories which have been proposed, that is, the sight theory and the theory of a general search." 1939. Karl von Frisch. "It is clear from a long series of experiments that after the commencement of the dances the bees first seek in the neighborhood, and then go farther away, and finally search the whole flying district....lt is thus seen that there is a biological function of flower scent not known before. The dancing bee can communicate a message about all kinds of scented flowers by means of the scent adhering to its body." 1960. Hans Kalmus (noted British bee researcher). "The way in which a bee which has found a rich source of nectar communicates this information to her sisters has puzzled beekeepers and naturalists for a long time. The explanation. however, is really quite simple; and any fairy tales about one bee telling the others, or leading the others to a locality, can be discounted. When a bee returns to the hive with her stomach filled with honey or nectar, she starts dancing on the combs in a characteristic way, beating her wings and thus spreading the smell of the flower which clings to her body. The other bees become interested by the dance and go searching for that particular smell." 1969. Wenner, Wells, and Johnson. "Our results support the olfaction hypothesis and contradict the dance language hypothesis. Recruits came to the site marked by the food odor, but not necessarily to the sites presumably indicated in the hive by the dance maneuvers of returning foragers." 1975. James Gould. "Von Frisch's controls do not exclude the possibility of olfactory recruitment alone, and Wenner is certainly correct in saying that an endless repetition of ambiguous experiments does not add anything to the evidence." 1980. R. Rosin (long-term critic of the dance language hypothesis). "We are now at a stage in the controversy where supporters of the 'dance language' hypothesis concede that honey-bees normally use odor alone." 1984. Ring Carde (eminent researcher in the field of odor orientation). "[That] the principal mechanism of 'long-distance' flying orientation to an airborne chemical stimulus in the wind is an opto-motor-guided, chemically-induced, upwind orientation (or anemotaxis) has gained wide acceptance as a considerable body of experimental evidence ... has accumulated." The above quotations highlight the importance of flower odor and/or wind patterns as newly recruited bees seek a food source already visited by their hivemates. Beekeepers might find it strange that I could find no inclusion of the above observations in any book or review of beekeeping or bee research published during the past few decades. How could that be? How could bee researchers and book authors omit information about a common behavior that beekeepers can see every day as they work with their colonies? To understand that dilemma, one must consider the means by which a person becomes a bee researcher. Most do so in an apprenticeship system. Instead of receiving an in-depth education in the process of science, a bee-oriented graduate student works in the laboratory of an established mentor. That student thereby becomes a member of what is known as a "thought collective" (e.g., Ludwik Fleck, as in Wenner, 1997), absorbing a "belief system" that will insure compatibility with other scientists in the field and success in the chosen career. Novice bee researchers can well remain unaware of the degree to which they may become biased by their mentors. Outsiders, though, can readily spot such a mindset by listening to what a novice may say and how it is said. For example, does a bee researcher use the expression, "the language" of bees or "their language" (both really interpretation, but viewed as fact), rather than the expression, "dance maneuver" or "waggle dance" of bees (observation or description)? Unfortunately, the published papers and books about bee behavior that students read contain little or no mention of the alternative odor-search hypothesis (e.g., von Frisch in 1939 - as in Wenner, 1993; Wenner and Wells, 1990). Not surprisingly, under the circumstances, those sources also fail to treat the importance of wind direction in colony foraging patterns, a topic covered by Friesen (1973) a quarter of a century ago. The Need for Scent in a Crosswind Experiment Von Frisch recognized that, without scent, one gets no recruitment. He wrote (see Wenner, 1993): In performing [my] experiment, I succeeded with all kinds of flowers with the exception of flowers without any scent. Compare that observation with a comment by Bogdany and Taber (1979, p. 58), "...a substantial number of recruits still found the food without odor being added." Who was correct? We have decided that von Frisch was apparently correct in his perception (see below), but others have conducted experiments and apparently failed to appreciate the fact that bees might perceive and orient to some odor other than that intended as a cue by the researchers. For instance, a strong odor of trampled vegetation or suntan oil could adhere to the bodies of foraging bees, odor that they would carry back to their hive (e.g., Wenner and Wells, 1990. pp. 132-134). Recruited bees could then search for odors associated with the experimenters or their activity. The researchers could thus gain a false impression that those searching bees had used dance maneuver information. Fortunately, with sufficient care one can exclude odors as a factor in studies of recruitment behavior and obtain results consistent with those reported in 1939 by von Frisch (see Wenner and Wells, 1990; Chaps. 8-10). Friesen (1973), for example, successfully excluded extraneous odors and obtained clear cut results. In one experimental series that ran for 11 days, he had 10 regular foragers flying crosswind from a hive to a station 400 yds away (360m - less than a 6 mm total round trip time for foragers), tallied every trip by each forager, and killed each new recruit upon arrival. Midway through each experimental period that ran for more than 4 hours each day, Friesen switched from scented to unscented food, taking care to clean all surfaces of any traces of the target odor used. The average number of round trips per 15 minute period remained high throughout the experiment (Fig. I), with only a slight dip in number of round trips with removal of scent. (Switching from scented to unscented food apparently confused some foragers momentarily.) |
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| Fig. 1. Average number of round trips made by ten foragers at a feeding site each fifteen minute interval during an 11 day period (after Friesen, 1973, Fig. 1). Ten regular foragers flew 360m from the hive crosswind to the feeder. Friesen replaced scented sugar solution with unscented solution at the end of two hours (arrow), resulting in only a little confusion for the foragers. |
| The unmarked bee arrivals during each 15 minute period (killed upon arrival) reveals much (Fig. 2). One can readily see that recruits did not begin to arrive until foragers had made a great many round trips (an average of 178 trips during the first 2 hours). However, the number of recruits (an average of only 27 recruits during those 2 hours) was only a small fraction of the number of round trips by regular foragers. Clearly, crosswind recruitment is difficult, even with odor provided. |
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| Fig. 2. Average number of recruit arrivals per fifteen minute interval during the 11 day forager visitation shown in Fig. 1. After the switch from scented food to unscented food, recruit arrivals dropped to near zero (arrow). |
| Friesen's removal
of odor from the food and thence from the locality at the end
of the first two hours produced a striking result (Fig.. 2).
Recruits suddenly ceased arriving at the dish presumably indicated
by foragers as they danced in the hive (and we already know that
less odor in the food leads to a greater frequency of dancing
in the hive - Wells and Wenner, 1971). Friesen justifiably concluded,
"Recruits were attracted to the odors from the food which
were carried by foragers and were dependent on these odors for
success." Of course, anyone could easily repeat that or a similar experiment within a couple of weeks during a nectar dearth and thereby test whether they themselves had successfully eliminated odor cues (see Part III of this series). Earlier we had obtained the same type of result in a 24-day sequential experiment (summarized in Wenner and Wells, 1990; Ch. 10). By using odor or no odor, we controlled the location at which bees arrived in the field - regardless of any direction information potential recruits supposedly had obtained before leaving their hive. In other experiments (e.g., Fig. 8.1 in Wenner and Wells, 1990), the presence of seemingly innocuous locality odors could mislead eager experimenters to conclude that recruitment had occurred even to unscented food. Few bee researchers realize that normal sucrose solution (table sugar), properly prepared, has no odor (i.e., the vapor pressure of sucrose solution equals zero). Hence, one must use an odor marker (deliberately or unwittingly) or searching bees cannot find the target dish. It is thus exceedingly difficult to demonstrate that searching bees have located the target source by using the dance maneuver information and not solely the odor used as a marker (or a contaminant such as someone's scented suntan lotion). To date, however, apparently no one has demonstrated that any searching bees "fly directly out" to the target food source (e.g., Wenner, 1998). All of the above becomes more apparent when we consider the rate of success and the amount of time necessary for a newly recruited bee to find a food source for which it is searching. After leaving the hive, naive bees spend a great deal of time searching for the target source, and very few of them succeed (see 1991 review by Wenner, Meade, and Friesen, as summarized in The American Bee Journal by Ed Southwick - October, 1992). Yes, searching bees can find a target source of food - but only if they have one odor cue or another as a guide. Also, odor molecules, being physical particles, can travel only downwind. As such, an insect, such as a moth, cannot "detect the odor (the sex pheromone) of a female [moth] at great distances, even at the rate of a single molecule in the air," as claimed by Taber in the May issue. Thus, wind direction, a factor nearly completely overlooked this past half century, is critical for the success of searching bees and, hence, must influence the foraging patterns of colonies. Parts II and III of this series will treat that topic more fully. Acknowledgements I thank Don Cole, Wyatt Mangum, Mike Polakoff, Justin Schmidt, Pat Wells, and others for their suggestions during preparation of this article. Literature Bogdany, F. J. and S. Taber. 1979. The significance of odor for bees orienting across a canyon. Apidologie. 10(1):55-62. Friesen, L. J. 1973. The search dynamics of recruited honey bees. Apis mellifera ligustica Spinola. Biological Bulletin. 144:107-131. Southwick, E. E. Bee research digest: Foraging, recruitment, and search behavior of honey bees. The American Bee Journal. 132:641, 42, 44. Wells, P.H. and A. M. Wenner. 1971. The influence of food scent on behavior of foraging honeybees. Physiological Zoology. 44:191-209. Wenner, A.M. 1993 [with K. von Frisch]. The language of bees. Bee World. 74:90-98. Wenner, A.M. 1997. The role of controversy in animal behavior. Pp. 3-37 in Greenberg, C. and E. Tobach (eds.). Comparative Psychology of Invertebrates: The Field and Laboratory Study of Insect Behavior. Garland Publishing, New York.). Wenner, A.M. 1998. Honey bee "dance language" controversy. Pp. 859-872 in Greenberg, C. and M. Hara, (eds.), Handbook of Comparative Psychology. Garland Publishing, New York. Wenner, A.M., D. Meade, and L. J. Friesen. 1991. Recruitment, search behavior, and flight ranges of honey bees. American Bee Journal. 31 (6): 768-782. Wenner, A.M. and P.H. Wells. 1990. Anatomy of a Controversy: The Question of a "Language" Among Bees. Columbia University Press. * Reprinted from Volume 138, No. 10, October, 1998 American Bee Journal |