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Bee Culture - October, 2000 - pages 6-7
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Scientists have puzzled for years on just how honey bees communicate. It has been amply demonstrated that ants, another social insect with remarkable similarities to bees, transmit information on food sources by odor. VonFrisch’s classical work seemed to show that bees communicate food source information through “language” - dances and sound. The language theory was questioned in the 1970s by Adrian Wenner who proposed that odor is indeed the means by which bees communicate food source information. A number of tests by Wenner supposedly proved his hypothesis.

Wenner’s work has been ignored or questioned by many in the scientific community but recent studies should put an end to the controversy.

Scientists in Belgium, using electron microscopes have discovered tiny etchings at the bottom of bee comb cells. At first, these marks were thought to be random, but careful study has revealed a true bee language. The markings are believed to be made by specialized workers that researchers have temporarily dubbed “Library bees.”

The markings appear to be of uniform size, like letters in an alphabet, and when run through a computer they fall into a pattern consistent with that of a language. Working day and night with high-speed computers, researchers have found that every hive or colony has a basic textbook or bee language, starting with a chapter on “Where do you go when you first emerge?” and including chapters such as “Pollen or nectar you decide” and “What to do on a rainy day.” These texts have been shown to be virtually identical among hives from widely different locations, although slight variations have been reported - in a colony from Africa, for example, a chapter entitled “Controlling aggression, good or bad?” was found.

Scientists are now looking at what appears to be a text at the bottom of queen cells entitled “The History of our Species.” One chapter of particular interest in this latest text has resisted efforts at decoding. but it appears to detail how bees have used mankind to spread their genes.

Needless to say, scientists are very excited about these latest discoveries which should put an end to the language controversy for all time. Significantly, Wenner has been noticeably silent on these new findings.

Submitted by Joe Traynor
Bakersfield, CA

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1994. Vadas, R.L., Jr. The anatomy of an ecological controversy: honey-bee searching behavior. Oikos (Forum Section). 69:158-166.
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Robert L Vadas, Jr., Ecosystem Research, Canadian Wildlife Service, Pacific & Yukon Region, P.O. Box 340, Delta, BC, Canada V4K 3Y3

“Variety is charming and not at all alarming.” (Old Essex Song)

“Relax! Were only between paradigm shifts anyhow.” (Crutcher 1991, p. 213)

“Lack of progress in science is never so much due to any scarcity of factual information as it is to the fixed mindsets of scientists themselves.” (Schram 1992, p. 357)

“Let them test their findings doubly and trebly before they regard any interpretation as certain. For often nature reaches her goal by another path, where man cannot see the way.” (von Frisch 1971, p. 90)

“Without well-conceived, critical experimentation, many evolutionary theories are little more than “Just-So” stories… The worry, then, is… that we will fail to imagine the full range of possible answers-hypotheses to test, or be unable to dream up clever ways to perform critical experiments (Gould and Gould 1988, pp. 123 and 225)

“But are there not more than enough bee books?… the unscientific reader will find it hard to tell where the observation ends, and the poetic fancy begins… I have been careful not to embroider imaginatively on the facts, which are poetic enough in themselves… Anyone who wants facts about the life of bees and not the picture of them painted by the creative imagination can look at the textbooks.” (von Frisch 1953, iii-iv)

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I review literature on the controversy of honey-bee searching behavior, specifically the clash between researchers supporting the odor-search versus dance-language hypotheses. Addressed problems include science philosophy, null models, analytical bias, experimental control, teleology, parsimony, ad hoc explanations, and censorship of scientific findings. Second, I review other literature on scientific philosophy to verify the commonness of these problems throughout the biologicai sciences.

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Overview of the honey-bee controversy

The history of behavioral research on honey bees (Apis spp.) has been most interesting from sociological and philosophical perspectives (Wenner 1971, 1989. Wenner and Wells 1987, 1990. Veldink 1989). Of particular controversy was whether recruited honey bees found food (nectar and pollen), water, propolis (tree-bud resin), and new nests by sensory processes alone (odor-search hypothesis), or by using dance-language information provided by scout bees that had already visited these resources (Lindauer 1971, Seeley 1985, Gould and Gould 1988).

Although honey-bee foraging was examined by Aristotle and other ancient scientists, intensive study did not begin until the 20th century (von Frisch 1953, 1971, Lindauer 1971, Seeley 1985, Gould and Gould 1988. Wenner and Wells 1990). Early researchers, and later K. von Frisch, favored the odor-search hypothesis, as honey bees were shown to use their antennae to obtain olfactory cues during nectar and pollen seaching. Soon, however, some researchers hypothesized that honey bees also communicated in the hive with their fellow workers, particularly because recruited bees often reached food sources without having to follow flying scout bees. Communication apparently occurred via two dance patterns; whereas a simple ’round dance’ was apparently adequate to recruit other worker bees to food sources near the hive, a ‘wagging dance’ was apparently necessary to give distance and direction information for farther foods (von Frisch 1953, 1971, Lindauer 1971). By midcentury, von Frisch and colleagues gathered what seemed to be convincing evidence in favor of the dance-language hypothesis for bee foraging, de-emphasizing earlier results on the importance of odor cues (von Frisch 1953, 1971, von Frisch and Lindauer 1956, Lindauer 1971, Wenner and Wells 1990). Von Frisch hypothesized that honey bees had more complex communication systems than did most birds and mammals, a counterintuitive idea that was at first shunned by the scientitic community, but later accepted by other bee researchers and biologists in general (Seeley 1985, Gould and Gould 1988, Wenner and Wells 1990). The honey bees were hypothesized to be intelligent creatures with photographic memories, space-age sensory and navigation systems, and possibly even insight skills, and von Frisch won a Nobel Prize for his findings (Lindauer 1971, Seeley 1985, Gould and Gould 1988, Wenner and Wells 1990). Contemporary bee-dance researchers such as J. L. Gould (Gould and Gould 1988, Gould 1992) and Seeley (1983, 1985, 1989, 1991) express little doubt that the dance language is an evolutionary adaptation for facilitating the foraging of bees in superorganismal fashion. Theoretical studies of honey-bee foraging behavior have thus been initiated by Seeley and colleagues (Camazine and Sneyd 1991, Bartholdi et al, 1993) to demonstrate that dances, competition, and optimal-foraging behavior among individual bees promote optimal foraging efficiency for the whole colony, via attainment of ideal-free distributions.

When A. M. Wenner and colleagues first began their honey-bee research in the early 1960’s, they accepted von Frisch’s dance-language hypothesis (Wenner et al. 1967, Wenner 1971, Wenner and Wells 1990). But as they performed experiments, they discovered several discrepancies with the prevailing paradigm (see below) and revived the odor-search hypothesis. Their criticism of the various experimental designs that had been used by von Frisch and other dance-language proponents highlighted the shortcomings of these tests and served to reinvigorate honey-bee research without dismantling the dance-language hypothesis (Lindauer 1971, Gould and Gould 1988, Wenner and Wells 1990).

To their surprise, Wenner and colleagues’ evidence supporting the odor-search hypothesis and criticisms of the dance-language hypothesis were at best ignored, at worst chastized and censored (Veldink 1989, Wenner and Wells 1990). To some extent, it became a ‘biopolitical’ battle of the personalities, with von Frisch and Wenner being viewed as the gracious hero and paranoid villain, respectively (Veldink 1989). Many scientists assumed that Wenner’s experiments were flawed, merely because they disagreed with von Frisch’s, even though von Frisch did not present his experimental methods until several years after he did his research (making it difficult for Wenner and other researchers to replicate these experiments). Hence, later researchers often committed the ‘appeal to authority’ and assumed that von Frisch’s dance-language hypothesis was fact, rather than viewing the data objectively and logically or performing their own experiments. The dance-language hypothesis became a paradigm through repetition in textbooks on animal behavior and sociobiology (e.g., Evans 1968) and honey-bee biology (Seeley 1985, Gould and Gould 1988).

The antagonism against Wenner impelled him to write a short book on the philosophical implications of the honey-bee controversy (Wenner 1971), and he switched his research field to marine invertebrates (Veldink 1989). But he did not give up the fight, expanding his philosophical perspective on honey-bee research to other biological topics and to scientific methodology in general (Wenner 1989, Wenner and Wells 1990). Wenner emphasized that scientists often were not objective, despite popular, stereotypic perception, and that several decades may often be required for biologists to shift away from nonviable hypotheses. That is, honey-bee researchers and other scientists were often susceptible to problems of ‘paradigm hold’ and ‘logical gap’ that Kuhn and Polanyi had earlier recognized; anyone who did not accept the prevailing paradigm was ostracized. Interestingly, Wenner and Wells’ (1990) book has been vehemently criticized by bee-dance researchers (Seeley 1991, Gould 1992), but other scientists have heralded the book as an important advancement in science that should be required reading for biologists in general (Slobodkin 1991, Massaro 1992, Rojot 1992, Schram 1992).

Interpretation of the honey-bee controversy

What went wrong in the progress of honey-bee behavioral research? First, there were problems with philosophical approach (Wenner 1971, Wenner and Wells 1990). Namely, (a) dance-language proponents did not formulate or adequately test alternative working hypotheses, particularly the odor-search hypothesis; and (b) their experimental tests were designed to verify the dance-language hypothesis, rather than to falsify it in Popperian fashion via ‘crucial’, unambiguous experiments (sensu Platt 1964).

Dance-language proponents did not give the odor-search hypothesis fair testing because they did not formulate realistic experimental expectations for this hypothesis (Veldink 1989, Wenner and Wells 1990, Rosin 1992). Namely, von Frisch concluded that honey bees did not use olfaction during foraging, because the bees did not need to open their abdominal Nasanov (scent) glands to stimulate other bees to forage nearby. However, this test showed only that the Nasanov gland did not recruit other foragers, and does not falsify the food-odor-search hypothesis. Rather, the function of the Nasanov gland is apparently to settle and orient swarming bees (during migrations to new hives) and dislocated bees of the colony, and not to strengthen food-site odors (Wenner 1992, Wells et al. 1993).

Typically, dance-language proponents used the verificatory mode in designing their experimental tests to demonstrate dance communication (Wenner 1971, Wenner and Wells 1990). Only Wenner and colleagues performed ‘crucial’ falsification tests, although some other researchers came close to performing decisive experiments. Namely, Wenner had noticed that extraneous odors, such as cut grass or researchers’ body lotions, affected the foraging movements of bees. These observations led him to develop a ‘crucial’ experiment to determine if worker bees could be recruited away from the experimental station if it was no longer scented, unlike the control stations. The answer was “yes”; recruited bees used odor cues, and not dance-language cues, to locate the food at the control stations.

In response to these two sets of experimental problems, Wenner and Wells (Wenner 1989, Wenner and Wells 1990, Wells 1991) advocated that a composite philosophical approach was needed, as advocated by such researchers as Platt, Chamberlin, and Popper later in his life. Neither falsificatory tests (early Popper approach) nor verificatory tests were adequate by themselves to advance honey-bee and other scientific research. Whereas the verificatory approach biased findings in favor of current hypotheses because scientists merely searched for confirming evidence, the falsificatory approach sometimes led to the opposite problem, because scientists merely searched for negative evidence and were thus throwing away potentially useful hypotheses. In statistical terminology (sensu Peters 1991), verificationists and falsicationists commit too many type-I and type-II errors, respectively, if the ‘alternate’ hypothesis is considered to be the ‘pet’ theory. Instead, a healthy mix of verification and falsification studies, as well as multiple working hypotheses, is needed; honey-bee hypotheses should have been efficiently tested with ‘crucial’ experiments and refined so that further tests and progress could have been made (cf. Platt 1964). This ’strong-inference’ approach is more flexible, multifaceted (pluralistic), and powerful for advancing scientific knowledge, and is more than a simple falsificatory approach (Wenner and Wells 1990).

The second problem was that null (random) mathematical models were not used by dance-language proponents in their experimental tests (Wenner and Wells 1990, Wenner et al. 1991), even though Wenner (1971) began using them in the late 1960s to criticize von Frisch’s ’single-control fan’ experiments. Namely, von Frisch and other researchers placed several food stations in a semicircle on the upwind side of the hive, the central (’experimental’) station being the one that scout bees were exposed to first (the other food cues were the ‘controls’). Hence, one might expect most bees to go to the experimental station merely because it was the center of the odor source, rather than being directed there by dancing bees, as schematized by Wenner’s mathematical model. These experiments also highlight the problem of nonrandom, biased placement of treatments and controls, similar to von Frisch’s early, mistaken hypothesis that sugar (nectar) and pollen foraging respectively elicit round versus waggle dances, based upon experiments with sugar dishes placed only near the hive (Gould and Gould 1988).

Wenner expanded his use of null models to test honey-bee hypotheses when he reviewed several studies showing that most bees search for food, water, and new hives close to their home hive (Wenner et al, 1991). That is, plots of the number of bees versus distance from the hive for a given colony usually gave a lognormal distribution (skewed right) regardless of where experimenters placed food cues. This is consistent with the odor-search but not the dance-language hypothesis, because the latter would predict different distributions depending upon where food was located. Wenner et al. (1991) suggested that the lognormal distribution may result from variation among individual bees and environmental variation during the expanding spiral (circle-out) searches of individual bees.

Third, von Frisch and other verificationists often ignored anomalous behaviors by honey bees, i.e., those that did not support the dance-language hypothesis and Nasanov-gland function in foraging (Veldink 1989, Wenner and Wells 1990, Rosin 1991, Wells et al. 1993). Most importantly, von Frisch disregarded his early evidence in favor of the odor-search hypothesis when he championed the dance-language hypothesis (Wenner and Wells 1990). That is, he had previously noted that worker bees follow the dancer around with their antennae touching the dancer’s body, and that flower scents adhere well to the honey bee’s body and may linger for several hours (Lindauer 1971, Seeley 1985, Gould and Gould 1988).

Moreover, when Wenner repeated von Frisch’s experiment to tilt honey-bee nests in order to distort the directional information of dances, the recruited bees still found food and apparently ignored the still-accurate distance information provided by the dancers: the recruited bees did not scatter in all directions as von Frisch had found (Gould and Gould 1988). Gould and Gould (1988) interpreted Wenner’s disparate results as an artifact of overly concentrated food solutions, which supposedly prevented bees from dancing (cf. Gould 1992). But such an interpretation was based on von Frisch’s disparaging comments of Wenner’s experiments, and not on empirical evidence per se (Gould and Gould 1988). Gould and Gould (1988) used a similar argument when Wenner redid J. L. Gould’s experiments with stronger food odors and found that recruited bees flew to food, rather than to the bare spot that scout bees were dancing for (in contrast to Gould’s results).

Furthermore, behavioral observations showed that recruited bees did not fly in ‘beelines’ to the food source as von Frisch had claimed; their routes were more circuitous (Seeley 1985, Gould and Gould 1988) and suggestive of search by odor, as in many other insects (Wenner and Wells, Rosin 1991). That is, bees typically flew down-wind from the hive, then zigzagged upwind towards food resources. Moreover, recruited bees that flew the correct distance (or direction) provided by dance information usually did not fly in the correct direction (or distance). Rather, most of the supporting research for the dance-language hypothesis was for the minority of bees that were successful in finding the correct feeding locations. Although Seeley (1985) and Gould and Gould (1988) still favored the dance-language hypothesis because even partial success might be worth something in a large bee colony, Wenner and Wells (1990) correctly criticized such data analyses for being biased in (statistically) unacceptable ways.

Fourth, dance-language proponents’ experiments were often confounded by lack of adequate controls (Wenner 1971, Wenner and Wells 1990). Recruited bees were often experienced foragers, i.e., aware of food and odor locations before being exposed to dances by scout bees. This would enhance the ability of recruited bees to find food sources even if they did not get any distance or direction information from the dances. As collectively emphasized by various bee researchers (von Frisch 1953, Lindauer 1971, Seeley 1985, Gould and Gould 1988), honey bees can memorize the odors, shapes, colors, opening times, and access points of flowers for their entire foraging careers.

Moreover, the “control” food sources (dishes) set out in single-control experiments were not adequate controls because they had not been visited (conditioned) by any bees, in contrast to the experimental station, which was visited by scout bees before their dances at the hive (Wenner 1971, Wenner and Wells 1990). Hence, possible odor cues left by scout bees needed to be at all feeding stations, which Wenner accomplished via ‘double-control’ (sham) experiments; the control dishes were allowed to be colonized by bees from other colonies. This increased the proportion of recruited bees going to the control stations after dances, evidence for the odor-search hypothesis.

Fifth, teleological reasoning and adaptive stories were inappropriately used to verify dance communication (Veldink 1989, Wenner and Wells 1990). Forager bees’ waggle dances did contain distance and/or direction information to food sources, albeit imprecise information, but this by itself does not prove that dancing or recruit bees are aware of this information. Rather, Wenner and colleagues (Wenner et al. 1967, Wenner and Wells 1990) found that sound production by dancing bees was better correlated with food distance than were dance movements, and Gould and Gould (1988) emphasized that sound production was necessary in dark hives to allow worker bees to follow dancing scouts. Nevertheless, Wenner et al. (1967) found that sound production was better correlated to temperature fluctuations than food distance. Similarly, the frequency of firefly flashes and cricket chirping increase with ambient temperature, and correlations between behavior and environmental condition are common in other insect species not considered to communicate with each other (Gould and Gould 1988, Massaro 1992).

Although von Frisch and other dance-language proponents assumed that bees would not waste energy dancing unless they were communicating, these researchers failed to consider alternative hypotheses (Jamieson 1986, Wenner and Wells 1990, Rosin 1992). For example, (a) the forager bees may dance as a reaction to harassment from other worker bees crowding around them (Rosin 1992); (b) they may dance to allow other bees to smell their bodies and learn the ‘hot’ odors (Wenner and Wells 1990); (c) the individual components of the dance may be adaptive, rather than the dance as an aggregate (Rosin 1992); and/or (d) the dance may reflect excitement, as honey bees are known to dance on newly found hives (Wenner 1992) and scouts of the more primitive stingless bees successfully recruit workers despite their undirected hive dances (von Frisch 1953, Lindauer 1971).

Sixth, many of these adaptive arguments were not parsimonious explanations of bee behavior. (1) Von Frisch (1953) himself noted that although honey bees showed retentive memory for colors and times that provided best foraging conditions, bee behavior was mostly stereotypic as a result of the bee’s small, primitive brain (cf. Wenner and Wells 1990). That is, the ability to communicate via dances probably would require extensive sensory integration (Lindauer 1971, Seeley 1985, Gould and Gould 1988). (2) Waggle dances took place on both vertical and horizonal surfaces, and in the dark and sunlight (von Frisch 1953, Lindauer 1971), such that worker bees would have to use their antennae (for dancer vibrations), proprioreceptors, and/or eyes, depending upon the circumstances, to translate the information in the dance (cf. Seeley 1985, Gould and Gould 1988). As worker bees are already known to touch the dancer with their antennae (von Frisch 1953, Lindauer 1971), it is more parsimonious to assume that tactile and olfactory cues alone are the information communicated. (3) It is unlikely that bee dances contain distance and directional information to new hives, because the scout bees fly out in circles around the hive (Wenner 1992). That is, the irregular flight paths of scouts may require sensory innovations much too complicated for translating this information to distance and directional information as the crow flies. (4) The bias of the recruited bees for the experimental station in single-control experiments was more than would be expected by the dance-language hypothesis, based upon the inaccuracy of bee dances for providing distance and direction information (Wenner 1971, Wenner and Wells 1990). Lindauer (1971) hypothesized (ad hoc) that worker bees averaged the information from several dances to achieve this superior accuracy, but this is neither parsimonious nor consistent with Wenner’s double-control experiments (see above).

Acceptance of the unparsimonious assumption that honey bees had extraordinary sensory and communication skills relative to other terrestrial insects and vertebrates may reflect bias by dance-language proponents, in their admiration for honey bees (Veldink 1989, Wenner and Wells 1990, Rosin 1992). Indeed, Gould (Gould and Gould 1988, Gould 1992) admitted that the odor-search hypothesis may explain much of the foraging behavior of honey bees, but pleaded that dance communication not be totally ignored as a possibility. However, use of parsimony (Occam’s razor) would eliminate the dance-language hypothesis for explaining bee behavior, particularly because (a) bee brains probably lack the infrastructure for higher-level sensation and communication, and (b) the odor-search hypothesis provides reasonable predictive power by itself.

And seventh, dance-language proponents used too many ad hoc explanations to explain away discrepant results, further intensifying the overuse of adaptationist, “just-so” arguments. For example, the dances of temperate honey bees (Apis mellifera) were known to give less accurate distance and direction information than dances of tropical (African) species (Gould and Gould 1988). But instead of downplaying the importance of A. mellifera dances in foraging, Gould and Gould (1988) suggested that such inaccuracy might even be adaptive. Namely, sloppy dances might spread recruited bees out across more flowers within a patch, given that patches should be larger and persist longer in the temperate than tropical zone. But swarm dances were just as inaccurate as food dances in A. mellifera, even though new nest sites were small in size unlike patches of flowers (Gould and Gould 1988). Again, instead of rejecting their adaptive story, Gould and Gould (1988) suggested that bees attended more swarm dances to better estimate where new nest sites were (via the above-discussed averaging hypothesis of Lindauer).

Another example of ad hoc explanations concerned the inability of honey bees to recruit to food sources on boats in a lake, despite extensive dances for the food by scout bees (Gould and Gould 1988). Only when the boat was moved closer to shore did bees find the food, such that Gould and Gould (1988) considered honey bees to be intelligent enough to “know” that scout bees dancing for sites in the middle of the lake were mistaken and to be ignored. Clearly, dance-language proponents indiscreetly used ad hoc explanations to stack assumption upon assumption and thus preserve von Frisch’s communication hypothesis.

In sum, Wenner (Wenner 1971, Wenner and Wells 1990) spearheaded a useful critique of a paradigm that had not been adequately tested, as such dance-language proponents as Gould and Gould (1988) were willing to admit. But the latter researchers still asserted that Wenner was mistaken about the irrelevancy of honey-bee dances for recruiting bees to food and other resources. As emphasized by Gould (Gould and Gould 1988, Gould 1992), Massaro (1992), and even Wenner and Wells (Wenner and Wells 1990, Wells 1991), different sensory processes may be used in different situations to find resources. Even if the odor-search hypothesis does apply most of the time, particularly when food odors are strong, it cannot be concluded that the dance is never important for recruiting bees. The point is, scientists cannot definitively prove or disprove an hypothesis with limited data, as I will further discuss below.

What bee researchers have not done, however, is to determine under what circumstances dances might be important for recruiting bees to food and other resources. While this approach is verificatory (ad hoc) rather than strict Popperian falsification, it would prevent an unceremonious discarding of an hypothesis that still may be of some use. But this means that dance-language proponents should stop attacking Wenner (e.g., Lindauer 1971, Gould and Gould 1988, Seeley 1991, Gould 1992) and begin designing tests to pinpoint the spatiotemporal scale(s) that dancing is useful as a communication tool. Until then, commercial bee keepers will continue to ignore the “ivory-tower” findings of dance-language proponents, because the research programme has not provided a predictive framework (sensu Peters 1991) that is useful for managing bees (Wenner and Wells 1990, Schram 1992).

Scientific problems in the ecological and behavioral sciences

Clearly, the honey-bee controversy brings to light several important guidelines for biologists and other scientists to make the research environment more habitable and productive. These include (1) the need for both verificatory and falsificatory approaches to balance research programmes; (2) the need for null (random) mathematical models to test alternative hypotheses; (3) examination of all relevant data, even if they contradict prevailing hypotheses; (4) the need for adequate controls and ‘crucial’ experiments; (5) avoidance of teleological reasoning to justify adaptive stories; (6) the need for parsimony and realism in assessing organisms’ mental and physical abilities; (7) circumspect use of ad hoc explanations; and (8) avoidance of scientific censorship.

To further understand the antagonism between proponents of the dance-language and odor-search paradigms, readers will have to delve into the honey-bee literature him- or herself. But a review of other scientific literature is appropriate here, to demonstrate that the honey-bee controversy is not atypical in biology.

First, the relative importance of verificatory and falsificatory approaches has been heavily debated by population (Cousens 1985, Calow 1987, Grime 1987, Mentis 1988), community (Poore 1962, MacFayden 1975, Saarinen 1980, Salt 1983, Elner and Vadas Sr. 1990), and theoretical ecologists (Haila 1988, Taylor 1989, Scheiner et al. 1993), evolutionary biologists (Van Valen 1976, Hull 1988), environmental biologists (Romesburg 1981, Murphy 1989, Eberhardt and Thomas 1991, Nudds and Morrison 1991), social scientists and statisticians (Tukey 1969, 1980, Tweney et al. 1981, Loehle 1987, Nesselroade and Cattell 1988), and science teachers (Zielinski and Sarachine 1990, Stinner 1992). Although several of these investigators argued for one approach over the other, many of them (particularly the social scientists and science teachers) accept both verification and falsification as complementary approaches that should be used hand-in-hand for generating and testing hypotheses. That is, exploratory (empirical or modelling) analyses to search for patterns and generate hypotheses, as well as synthetic, inductive reviews that establish which patterns are general and applicable in given situations, are valid verificatory approaches. Likewise, Popperian (’hypothetico-deductive’ or ‘confirmatory’) analyses that test whether a given pattern is present in a new data set, or that test predictions to be expected if a given ecological mechanism is operating, are valid falsificatory approaches. Descriptive and experimental scientists need not operate only in verificatory and falsificatory modes, respectively (Nudds and Morrison 1991). For example, descriptive data can be used to falsify ecological theories (Shipley and Keddy 1987, Vadas Jr. 1990a, Douglas and Matthews 1992), whereas dance-language experimentalists often worked in verificatory modes to examine honey-bee behavior (see above).

Moreover, the complexity of interactions between species and the hierarchy of factors affecting species suggests that strictly falsificatory approaches cannot be used because of the uncertainty of what biological (rather than statistical) hypotheses are being tested (Saarinen 1980, Bradley 1983, MacNally 1983, Underwood 1986, Matter and Mannan 1989). That is, correlation rather than causation is established by most descriptive and experimental studies (Wenner et al. 1967, Peters 1991). For example, in experiments in which one species depresses the abundance of another, natural-history observations would be necessary to determine if predation, competition, and/or other mechanisms was responsible for the changes in species’ abundances. Similarly, the consistency of empirical data with theoretical predictions does not prove that the ecological mechanisms built into the model are actually operating (Slatkin 1983).

Wildlife biologists (Romesburg 1981, Nudds and Morrison 1991) and community ecologists (Strong 1980, Connor and Simberloff 1986) in particular have criticized biologists who infer ecological mechanisms from patterns; this improper use of induction has been distinguished by the term ‘retroduction’ (Romesburg 1981, Nudds and Morrison 1991). Clearly, a single verificatory or falsificatory test done by ecologists and other organismal biologists cannot definitely make or break an hypothesis as easily as in the physical sciences and molecular biology (cf. Platt 1964), because of the greater spatiotemporal variability of patterns and quantitative ambiguity of theoretical predictions for the former softer, less mature sciences (Hammond 1978, Loehle 1987, Peters 1991). That is, scientists often make inductions (inferences) without enough replication of experimental or descriptive data to properly verify or falsify hypotheses (Hacking 1981, Hurlbert 1984, Loehle 1987), particularly because a pattern falsified at one spatial, temporal, or biological scale may be a valid pattern at other scales (O’Neill et al. 1986, Murphy 1989, Romesburg 1989, Vadas Jr. 1989, Peters 1991). Clearly, not all science is or should be based upon preconceived (biased) notions and hypothetico-deductive reasoning (Brush 1974, Mentis 1988), nor should new hypotheses be disregarded simply because they have not been properly tested yet (Loehle
1987).

Second, the use of null models has become important for testing whether nonrandom ecological and evolutionary phenomena (e.g., competitive exclusion and catastrophy-induced extinctions) are plausible (Raup 1977, Strong 1980, Gould 1981, Connor and Simberloff 1986). Although many of these “null” models involve assumptions that detract from what one might expect under random conditions, they are nevertheless laudable attempts to quantitatively test whether alternative, less parsimonious models are necessary to explain patterns in nature (Peters 1991).

Third, scientific revolutions cannot occur unless researchers stop ignoring and suppressing anomalous results and alternative hypotheses (Hacking 1981, Loehle 1987, Crutcher 1991, Peters 1991). Unfortunately, biologists and physical scientists often lack proper objectivity when undertaking and writing up research, because of their preconceived notions of how the world works (Brush 1974, Jackson and Prados 1983, Cole 1985, Erman and Pister 1989, Keddy 1990, 1991, Underwood 1990), although fraudulence itself is rather rare in science (Hull 1988). Admittedly, it is self-defeating to throw away theories because of occasional anomalies, because such anomalies could be the result of experimental error or be restricted to specific conditions (Ballard and Sparberg 1962, Poore 1962, Loehle 1987), and successful biological theories are often built from older, outdated ones (Hacking 1981, Stamp 1992). Nevertheless, models should not be mindlessly bandaged with ad hoc explanations when they clearly have little predictive power (Hacking 1981, Keddy 1991, Peters 1991). Scientific judgment and statistical analyses are clearly crucial for deciding when to discard old theories for new ones (Peters 1991).

Fourth, adaptationist stories have fallen into disfavor in evolutionary biology and sociobiology because teleological reasoning and theory are not good substitutes for observational and experimental data (Gould 1977, May and Robertson 1980, Stenseth 1983, Peters 1991). That is, one cannot validly assume that behavior is adaptive to corroborate theories, although teleological reasoning can have heuristic (and verificatory) value in generating hypotheses about functional adaptations (Ruse 1989). In particular, optimal-foraging behavior at the individual and population levels is energy-expensive because of the brain capacity and psychic power required, and thus unlikely unless there are strong selection pressures for optimal behavior (Westman 1977, Schmid-Hempel 1985).

Fifth, parsimony (Occam’s razor) is well-accepted as a tool in ecology and evolutionary biology, to keep hypotheses simple when greater complexity is unnecessary to explain ecological patterns and mechanisms (Holsmger 1981, Hull 1988, Peters 1991, but see Dunbar 1980). Moreover, concepts that are too complex and ambiguous to test properly should be replaced with operational, simpler theories that allow falsificatory tests to be done (Fryer 1987, Elner and Vadas Sr. 1990, Peters 1991).

And sixth, censorship of manuscripts and proposals is common in the biological and physical sciences (Barber 1961, Jaksic 1985, Peters 1991). Pielou (1981) and Wenner and Wells (1990), for example, noted that censorship of papers such as theirs took several forms, which I can corroborate based upon attempts to publish an anti-paradigm paper on competition theory (Vadas Jr. 1990b) and a “backburner” manuscript on fish ecomorphology. Namely, reviewers (or editors alone) may criticize and reject a single manuscript because it is “all” of the following: wrong and unscientific (critic #1), too controversial (critic #2), hackneyed because it merely provides common knowledge (critic #3), and boring because it addresses a dead topic that nobody cares about anymore (critic #4). Such bias is particularly apparent when a critic’s comments are caustic, contradictory, or do not otherwise make sense. Unfortunately, the same scientist may be a censor in one situation and the victim of censorship in another, such that it is hard to discern the heroes and villains (Barber 1961).

Censorship takes several forms in the biological and physical sciences (Barber 1961), most of which are apparent in the honey-bee controversy. (1) ‘Methodological bias’ is discrimination against theoretical, mathematical, or abstract approaches to science (Barber 1961). We could add here antagonism between descriptive and experimental biologists (Diamond 1983, Hart 1983, Wilson 1989, Underwood 1990), analytical and simulation modellers (Hall and DeAngelis 1985), reductionists and holists (Dunbar 1980, Saarinen 1980, Ulanowicz 1986), pheneticists versus cladists in systematics (Hull 1988), and honey-bee researchers that use strong food odors versus those who use weak odors (see above). (2) ‘Religious bias’ is discrimination against such ideas as Darwinian evolution and the ‘big bang’ theory of cosmology (Barber 1961). We could add here societal and cultural biases, which are particularly prevalent among ecologists (Risch and Boucher 1976, Smith 1978, Keddy 1990). For example, it is quite possible that dance-language proponents and opponents (such as myself) have socialistic and agnostic biases, respectively. (3) ‘Authority bias’ causes scientists to accept the views of older, respected scientists, i.e., the appeal-to-authority fallacy (Barber 1961, Dayton 1979). Ancient ecological data (e.g., animal population size from pelt counts) and authoritative reviews (textbooks, review papers, and popular-science articles) are often accepted uncritically, particularly by researchers outside the immediate research field and laypeople, worsening the paradigm hold (Gilpin 1973, Forman and Russell 1983, Elner and Vadas, Sr. 1990). Veldink (1989) and Wenner and Wells (1990) clearly documented these problems in honey-bee research (see above). (4) ‘Xenophobic bias’ causes researchers in one research field, society, or ’school’ (clique) to reject outside views (Barber 1961). This bias hurts multidisciplinary efforts and is typical of ‘normal science’, during which the status quo is stable against scientific revolutions (Hacking 1981, Tweney et al. 1981, Crutcher 1991, Romesburg 1991). In the honey-bee controversy, Wenner became an outsider when he started publishing negative evidence for the dance-language, causing other bee researchers to exclude him from scientific meetings and to reject his manuscripts (Veldink 1989, Wenner and Wells 1990).

Coda

To synthesize, much of the problems faced by Wenner and colleagues (Wenner 1971, 1989, Wenner and Wells 1987, 1990) in their attempts to test the dance-language hypotheses of honey bees are common in biology and science in general. Fortunately, bias and censorship are less common among scientists than among laypeople (Pease and Bull 1992), but it is ironic that scientists, particularly biologists, are often their own worst enemies when it comes to attacks upon science (Barber 1961, Rosenzweig et al 1988, Peters 1991). Nevertheless, examination of other research fields such as community ecology (but see Risch and Boucher 1976, Smith 1978, Keddy 1990), systematics, and evolution suggest that ‘religious’ and ‘authority’ biases are not always prevalent among biologists (Hull 1988). And although researchers in opposing camps may be more likely to tests opponents’ hypotheses in falsificatory fashion and give unfairly negative critiques of opponents’ grants and manuscripts, systematists have often been more evenhanded (objective) in their actions (Hull 1988). On the other hand, important ecological papers have sometimes been unfairly rejected by early reviewers (Cook 1977), and experimental manuscript submissions have corroborated the importance of reviewer bias against evidence contradictory to prevailing paradigms (Loehle 1987). Hence, the problems emphasized by Wenner and Wells (1990) in honey-bee research are applicable to at least some other scientific fields. Nevertheless, to avoid making inferences on limited case studies, further philosophical studies by biologists and sociologists are needed, because most science philosophers have focused their efforts on physical scientists (Warren et al. 1979, Tweney et al. 1981, Loehle 1987, Veldink 1989, Stinner 1992). Certainly, Wenner and Wells (1990) have made a good start in this direction, as have Saarinen (1980), Salt (1983), Hull (1988), and Peters (1991).

Acknowledgements - Helpful critiques of manuscript drafts were provided by P. L. Angermeier, C. A. Dolloff, R. W. Elner, W. E. Ensign, J. M. Morton, J. J. Ney, D. J. Orth, M. J. Sabo, R. L. Vadas, Sr., C. Veldink, P. H. Wells, A. M. Wenner, and Yrjo Haila, R. Vadas, Sr., P. Wells. A. Wenner also gave me several relevant reference materials. I thank the Dept of Fisheries and Wildlife Sciences (Virginia Tech) for its financial support during writing and revising of the manuscript. I also thank D. E. Gill, G. Morrison, and L. A. Nielsen for their stimulating graduate seminars on science philosophy, and the Univ. of Michigan biologist who unintentionally introduced me to the problems of censorship and dogmatism in science during 1986.

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“The common expression “I’ll believe it when I see it” is not necessarily true. Indeed, the converse is often more correct because we have a hard time seeing what we don’t believe.”

Norman Uphoff and Jerry Combs,
Cornell University

The 2006 March and April issues of the American Bee Journal included a two-part series by Emily Smith and Gard Otis entitled, “The ‘Dance Language’ of the Honey Bee: A Controversy Revisited,” and “Resolution of a Controversy: Functionality of the Dance Language of the Honey Bee,” respectively. The authors built a rational case for the “truth” of “bee language.” However, rational does not mean exclusive when it comes to interpretation - especially if one does not agree about the importance of Occam’s razor in this case (”Of two competing theories or explanations, all other things being equal, the simpler one is to be preferred”). The odor-search hypothesis for honey bee recruitment to food sources (initially advocated by von Frisch and later by us) is far more simple than the extra natural notion of bee language.

The authors failed to realize that bee language advocates have unwittingly undermined their case these past three decades, due to their repeated attempts to prove their belief system true (sort of like “crying wolf”). A single “proof” should have sufficed - multiple attempts at “proofs” implicitly reveal/admit failures of earlier proofs.

The absolute certainty expressed by the authors reminds me of a mid-1960s visit to our campus by Ronald Ribbands, esteemed bee researcher from Britain and author of the influential 1953 volume, The Behaviour and Social Life of Honey Bees. He spent several days with us while we conducted some of our double-controlled experiments (as summarized in Ch. 9 of our 1990 Columbia University Press book - Anatomy of a Controversy).

Ribbands observed the conduct of our experiments with great interest, saw no problems with their design or execution, but could not accommodate those results within his grasp of reality, results that contradicted implicit expectations of the bee language hypothesis. We debated the implications but could not agree on interpretation of those clear-cut results. Finally I thought to ask, “Do you think it conceivable that honey bees do not have a “language”? He responded immediately, “No, that is not possible.” We had a great time together during the remainder of our visit, because we understood that we “lived in different worlds” on the matter. Neither of us had a question about the evidence but differed on our attitude toward that evidence. It eventually became obvious that, by the time of the Ribbands’ visit to our campus, the bee language hypothesis had already evolved into dogma - a strong paradigm hold or “fact,” as it were.

A decade ago one of the “robot bee” researchers from Germany visited my office. He had brought a number of reprints that we went over together. As we looked at one reprint, I pointed out that the results in one of his tables of data did not conform to expectations of the language hypothesis. My comment fell on deaf ears; instead, he said, “Here, let me show you some other results.” His attitude remained dismissive when I showed him results obtained by both bee language advocates and by us that clearly did not fit the language hypothesis.

In 1935 Ludwik Fleck published a book, Genesis and Development of a Scientific Fact (later translated into English). In that text he used the phrase, “thought collective” to denote a community of scientists who mutually exchange ideas or maintain intellectual interaction. Such collectives then become intellectual prisons of sorts, because, in Fleck’s words, “The individual within the collective is, never, or hardly ever, conscious of the prevailing thought style, which almost always exerts an absolutely compulsive force upon his thinking and with which it is not possible to be at variance.”

Later, Thomas Kuhn (in his 1962 book, The Structure of Scientific Revolutions) expanded upon Fleck’s ideas with his use of the terms paradigm hold and paradigm shifts. That is, scientists unwittingly become locked into a prevailing theory to such an extent that they can no longer recognize other alternatives. As Fleck emphasized, social constraints also play a large role in that fixation to prevailing thought.

Fortunately, we had become aware of Kuhn’s writing at the time we were first gaining evidence at variance with the dance language hypothesis and had begun to appreciate the rough road ahead if we persisted with our “heretical” objections to that hypothesis. At the same time we also began to appreciate that this controversy had the potential to become a classic case of how science proceeds - as against notions many scientists hold about how they conduct their research.

However, we had no idea of the intensity of opposition we would face, even from such esteemed thinkers as E.O. Wilson (in 1969 and 1972) and Richard Dawkins (in 1970).

Robert Park wrote in his 2000 book, Voodoo Science, “The more persuasive the evidence against a belief, the more virtuous it is deemed to persist in it.” That is why those who endorse prevailing thought (dogma) gain accolades from the scientific community. In 1975 Paul Feyerabend assessed the situation as follows: “Popular science books spread the basic postulates of the theory; applications are made in distant fields, money is given to the orthodox and is withheld from the rebels. More than ever the theory seems to possess tremendous empirical support.”

It seems that the authors of the recent ABJ two-part series had begun (and had conducted) their review of the literature under the dance language paradigm hold. They summarized all the positive evidence they could glean from various contributions but failed to provide a balanced summary of all other available evidence. In doing so, they failed to see the forest for the trees; namely, any true resolution must be inclusive of all available evidence, not merely an advocacy of a particular hypothesis.

Science philosopher Karl Popper addressed that point: “It is easy to obtain confirmations, or verifications, for nearly every theory - if we look for confirmations.” Popper also wrote, “A theory which is not refutable by any conceivable event is non-scientific. Irrefutability is not a virtue of a theory (as people often think) but a vice.”

The authors’ choice of the word “resolution” was thus indeed unfortunate, as were their phrases, “the dance language” and “functionality of the dance language.” Those expressions reveal a deep-seated bias, an eagerness on their part to establish bee language as “irrefutable truth,” never again to be open to challenge. In that approach, they followed in the same vein as that of sociologist Eileen Crist (”Can an Insect Speak? - The Case of the Honeybee Dance Language”). Her paper was written under the tutelage of James Gould and Donald Griffin, both long term committed advocates of bee language.

The authors’ use of the word “resolution” would imply that we now have a theory of honey bee recruitment to food sources, a theory that accommodates all available results (the meaning of the word), but that is clearly not the case. That word also suggests that one must no longer challenge “prevailing” theory - one must believe in bee language as fact - that a mere insect can possess such an extra natural ability.

Notice that the authors used the term, “the dance language” throughout their presentation (as was true in the Crist article). Note here, then, an important distinction - “the dance maneuver” is fact (it does occur), but “the dance language” is interpretation (for which there is much supportive evidence but also much compelling negative evidence). Furthermore, one cannot merely dismiss or ignore negative evidence not in keeping with a hypothesis. Neither does an “overwhelming body of positive evidence” make a hypothesis irrefutable, especially when a large body of negative evidence remains unexplained.

The term, “functionality of the dance language,” is by far the most interesting aspect of their presentation. Whenever I have given a talk on our findings about the overwhelming importance of odor during recruitment of naïve bees to food sources (the Occam’s razor approach), the first question raised during the discussion period has nearly always been, “But, then, why do bees dance?” The authors apparently now seem convinced that they have resolved that teleological question. It would appear, in their minds, that the bee dance maneuver has distance and direction information in it “in order to send hive-mates to food source locations in the field.”

It is here that one can recognize a striking parallel between the bee language/odor-search controversy and the “intelligent design”/evolution controversy. Both are characteristic of belief systems - once something is known to be true, that idea is no longer open to question. That is, intelligent design people (creationists) claim that life is too complicated to have arisen by normal chemical/biological processes. Bee language advocates claim that the dance maneuver is too complicated to not have some “purpose” and could not be a functional-less activity (presumably “intelligent design” or its equivalent).

The dance language hypothesis rests upon an assumption that honey bees have special capabilities above and beyond those possessed by all other insects. The odor-search hypothesis of von Frisch and later re-formulated by us requires no special equipment on the part of bees. If we apply Occam’s razor to the question, there is no contest.

Is, then, the controversy “finally laid to rest” or “resolved” as Crist and the current authors have claimed? No, although a bee language belief system remains firmly entrenched in some quarters (as elucidated by Feyerabend, above), an accumulation of negative evidence from many experiments continues to erode unquestioning faith in bee language.

By contrast, attention to the overriding importance of odor during recruitment of bees to food sources should eventually yield rich rewards not anticipated by bee language advocates - rewards that have remained elusive under the dance language paradigm these past several decades.

Adrian M. Wenner
967 Garcia Road
Santa Barbara CA 93103
wenner@lifesci.ucsb.edu

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: wenner@lifesci.ucsb.edu
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.

References

Wenner, A.M. [with K. von Frisch]. 1993 [1937]. The language of bees. Bee World. 74:90-98. (http://www.beesource.com/pov/wenner/bw1993.htm)

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. (http://www.beesource.com/pov/wenner/abjnov1998b.htm)

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. (http://www.beesource.com/pov/wenner/az1991.htm)

See also: (http://www.beesource.com/pov/wenner/index.htm)

10 June 2005

Once again we are treated to a presumed final proof of bee “language.” The latest effort (”The flight paths of honeybees recruited by the waggle dance”) appears as a letter on pages 205-207 in Nature on 12 May 2005 by J. R. Riley, U. Greggers, A. D. Smith, D. R. Reynolds, and R. Menzel. Is the question of bee language now resolved? Hardly, because the nearly four-decade old controversy does not revolve about evidence - as will be documented in this treatise.

Ruth Rosin recognized that element of the problem when she posted (6 June 2005) the following comment (in part) on the honey bee e-mail network (BEE-L):

“The Nature (2005) radar-tracking study by Riley et al. has already created considerable excitement in the popular scientific news-media. The study, nonetheless, never did, nor could, salvage the dance language hypothesis, because the whole study is simply totally irrelevant to the dance language controversy”

“According to the report only 2 bees, (out of the 19 radar-tracked bees released near the hive, for which flight-tracks are provided) “landed at the feeder.” In response to questions about various details concerning the study, Uwe Greggers (the scientist who actually designed the study, however, informed me, among others, (in e-mail exchanges), that those 2 bees did not actually land at the feeder. Instead, they only landed on the stand on which the feeder stood, but never found the food, or the feeder (even when they were not more than 8 cm away from the feeder). Anyone who questions that is free to personally check with him.

Two days earlier she had also written to me (in part):

“There is, however, another, much more basic problem with the Nature (2005) study. The whole study is simply totally irrelevant to the DL controversy. Before seeing the published report I assumed that the experimenters did what they should have done first and foremost, i.e. radar-track recruits recruited by foragers feeding on scented food; which is what foragers invariably do in nature. It turns out that the experimenters did exactly the opposite. They strove very hard, and apparently succeeded in radar-tracking only bees that never found any food.”

“The honeybee DL hypothesis was intended to provide an answer to the problem how honeybee recruits find their foragers’ food-source, and other sources with the same major odor, in the field. In no way is it possible to provide any answer to such a problem by studying only bees that never found any food during the study. Since the whole study is totally irrelevant to the problem, any results obtained in the study cannot be relevant to the problem, either.”

A Broader Problem

During the past 35 years, the dance language controversy has centered on the question, “Can someone prove a hypothesis true and expect that hypothesis to become a fact, a fact no longer open to question?” Bee language advocates would have us believe so. Those who study scientific process feel otherwise.

We published the results of our double controlled and strong inference experiments in the late 1960s and 1970s, results that did not mesh with predictions of the dance language hypothesis (see below). Ever since then, research on honey bee recruitment to food crops has remained in a crisis state, with millions having been spent on efforts, in various series of experiments, to “prove,” once more, that bee language is real. In each attempt, bee researchers have admitted that previous attempts had not sufficed - but did so only after they felt certain that their own efforts had succeeded.

The recent radar tracking studies of bee flight paths that left the hive is just one more in such a series of attempted “proofs.” On 14 October 2003 James Fischer posted the following statement on BEE-L, one made by those involved in that radar research:

“We have used harmonic radar to measure the flight trajectories of bees recruited after observing the waggle dance, this has enabled us to settle (hopefully once and for all) this controversy in favour of Von Frisch.”

In the first few words of their 2005 Nature report, the radar tracking researchers also used the phrase, “the dance language” of bees instead of more objective phrases, such as: “the waggle dance,” or “the dance maneuver.” It became clear soon thereafter in their letter that they had started their experiments with the assumption that bee language is real and then had tried to prove it true (circular reasoning?).

The renowned science philosopher Karl Popper would have been appalled at such a brazen and naïve approach. For instance, in 1957 he stated: “It is easy to obtain confirmations, or verifications, for nearly every theory - if we look for confirmations.” In scientific experimentation, the easiest one to convince is oneself. That is why we need blind, double controlled, and other rigorous designs in experimentation - elements lacking in the present study.

Background Information

Karl von Frisch abandoned an earlier odor-search hypothesis and proposed his dance language hypothesis in 1946, a conclusion that rapidly became accepted nearly universally (including by me for my doctoral studies in the 1950s). That hypothesis provided a rational (though not exclusive) explanation about how newly recruited bees might manage to find a food source exploited by regular foragers. His interpretation morphed into the status of fact (”proved” or “discovered”), rather than remaining in people’s minds the hypothesis that it was.

What few appreciate today is that von Frisch’s language conclusion was at odds with his earlier published results and conclusion; that is, recruited bees use odor, and only odor, after leaving their parent colony in search of the crops exploited by experienced foragers. In 1937, for instance, he wrote:

“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”

For more information on that point, please access:

http://www.beesource.com/pov/wenner/bw1993.htm

The exotic notion of bee “language,” though unproven and lacking rigorous experimental tests, eclipsed von Frisch’s earlier odor-search hypothesis. One prominent bee researcher, H. Kalmus, held out. He wrote in 1960 (Simple Experiments with Insects. Doubleday & Company, Inc. Garden City, NY. p. 96):

“The explanation [of how a forager communicates this information], 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 she starts dancing on the combs 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.”

That comment by Kalmus thus matched the firm conclusion von Frisch had published in 1937.

Although I conducted my doctoral research in the 1950s with the belief in bee language, later experiments by my co-workers and myself yielded results clearly at odds with that hypothesis. A series of unfortunate and unexpected events (for example, see http://www.beesource.com/pov/wenner/aoac.htm) led us to execute rigorous experimental tests of the language hypothesis during the 1960s, the first such real tests ever conducted. (For clarification, experiments designed to gain support for a hypothesis do not count as tests.)

The first set of experiments involved a double control design. Bees from one hive foraged at only one station in a set of four; bees of another color foraged at all four stations. In contrast to predictions of the dance language hypothesis, recruits from both hives ended up in equal proportions at the four stations, despite the wide disparity of information presumably provided by dancing bees in the two hives. For details, see:

http://www.beesource.com/pov/wenner/scifeb1967.htm

http://www.beesource.com/pov/wenner/scifeb1967b.htm

The second set of experiments involved only one hive. In that case, a constant set of marked foragers imbibed scented sugar solution at two stations for 3 hours each day during a 24-day period. All unmarked bees were caught and tallied during that period. On some of the days, we switched to unscented food at the target stations but provided the scented food at a third station.

On those subsequent days, recruited bees ignored the dance maneuver information in their parent colonies and arrived, instead, at the third station where we had used scented food that had been provided on the previous day. For details see:

http://www.beesource.com/pov/wenner/sci1969.htm

Those sets of experiments are straightforward (with mutually exclusive designs) and the results should have been heeded. That did not happen. Instead, bee language proponents (by then, their numbers were legion) erred most seriously in two ways, errors repeated up to the present time:

1) Language advocates ignored Karl Popper’s caution: “Some genuinely testable theories, when found to be false, are still upheld by their admirers - for example, by introducing ad hoc some auxiliary assumption, or by re-interpreting the theory ad hoc in such a way that it escapes refutation.”

2) Language advocates apparently accept as valid only evidence that supports the von Frisch hypothesis. It appears that they consider counter evidence just “noise” in the system.

Back in 1865 Claude Bernard admonished against falling into such error: “[The experimenter] must never answer for [Nature] nor listen partially to her answers by taking, from the results of an experiment, only those which support or confirm his hypothesis.”

In short, during the past few decades, bee language advocates have repeatedly committed the error of only focusing on supportive evidence, while ignoring or discounting other evidence that does not fit within their “belief system.” That is, only positive evidence counts.

Flaws in “Proof” Experiments

During the past few decades we have seen the same mistakes occur repeatedly; language advocates have sought and embraced supportive evidence and dismissed negative evidence in an almost pathological manner. Any new supportive evidence always received wide acclaim, with great fanfare in the media (the exotic sells). Manuscripts submitted in support of the language hypothesis became published readily. Grant proposals that might yield positive evidence received funding. In fact, during the past several decades, millions have been spent on efforts to “prove” the language hypothesis true, once and for all.

Time in Flight and Success Rate for Searching Recruits

First came the results of some experiments by three undergraduates (Gould, Henerey, and MacLeod) that actually yielded results that did not mesh with predictions of the language hypothesis.

For example, they had marked with individual numbers a couple of thousand bees in the hive. They recorded 277 that left the hive after contacting a dancer. Of those, only 37 found either one of the two stations located in opposite directions from their hive. However, a third of those ended up at a station in the exact opposite direction from which the dance maneuver had presumably indicated the food location. Nevertheless, they concluded that attendant bees had used direction information obtained from the dancing bee. Despite that serious discrepancy, the journal (Science) would not permit us to publish a rebuttal (see: http://www.beesource.com/pov/wenner/EXC.htm).

“Misdirection” Experiments

Next came James Gould’s “misdirection” experiments. By shining a bright light at an angle to dancers in the hive, he reportedly changed the direction of the dance maneuver. For his first publication in that series (Nature 1974), in support of bee language, he included the results of only three of the 33 half-hour runs he had run. While first hailed as “elegant,” it later became apparent that the small sample sizes in his experiment and repeated publication of the results of his experiments in different display formats grossly exaggerated the importance of his contribution. Neither has anyone successfully repeated his experiments.

Mechanical Bee Experiments

After people finally became disenchanted with Gould’s results, researchers in Germany and Denmark published (with much fanfare) the results they had obtained by use of a mechanical bee (”robot” bee). They also claimed that they had obtained the final resolution of the controversy. Once again, though, it became apparent that they had not resolved the matter after all. They had to use odor in their experiments in order to obtain recruitment. (Without odor, there is no recruitment, just as von Frisch observed.) In one experiment, two real foragers plying between hive and station resulted in 50 recruits showing up at the test station. By contrast, only two recruits finally arrived at the feeding station after numerous bees had attended a robot bee. Support for their conclusions gradually faded.

It is no wonder that the honey bee dance language controversy has now persisted for nearly half a century. Others conducted less exotic studies during the past few decades and claimed that they had successfully resolved the issue of bee “language.” As usual, though, they tailored their experimental designs toward gaining supportive evidence for the hypothesis - rather than conducting true tests of that hypothesis.

Radar Tracking of Recruited Honey Bees

The latest “high tech confirmation” experiments involved radar tracking of recruited honey bees. Once again we see the usual pattern: a small sample size, biased researchers, much media splash, and dogmatic conclusions. Never mind that the evidence doesn’t fit the original hypothesis; they now considered that they had obtained “proof” of bee “language.” In an interview with a science reporter for the San Francisco Chronicle, for example, the lead scientist of the radar tracking project was quoted as insisting: “‘no really sensible person can come to any other conclusion’ than that von Frisch was right.”

In their experiments the radar tracking researchers made some serious errors in approach. Consider some background. The researchers had some bees trained to fly out to a feeding station and saw them later dance. They followed a bee that attended such a dance, caught it as it left the hive, attached a transponder onto its body, released it, and then followed the path of that bee with radar. To conduct their study they embraced a number of assumptions:

1) That a bee attending a dancer has the neurological/physiological equipment to obtain abstract physical information from another bee.
2) That such a particular bee leaving a dancer “intended” to travel to the “target” site (that experimental bees had gained a route memory of the feeding station relative to the hive).
3) The capture of a bee and fastening a transponder onto it doesn’t interfere with its presumably “programmed” behavior.
4) That the released bee flight path has only one explanation (in favor of “language,” in this case).
5) That they worked in an “odor free” area (odor free to bees) for their experiments.

From the account published in Nature, it appears that some critical controls were missing, including:

1) Flight paths of bees that had been similarly treated but had not attended a waggle dance.
2) Flight paths of departing bees that had attended a waggle dance that had visited food located in a different direction.
3) Flight paths of bees searching for a scented food source (as pointed out by Rosin, above).

That is, the reasoning seems to be: if the escaping bees fly off in the “right” direction (the only direction arranged for), then they have used their language.

All of the above reminds me of a 1971 statement by Nobel Laureate Albert Szent-Gyorgyi (biochemistry): “If you know in advance what you are going to do, or even to find there, then it is not research at all: then it is only a kind of honorable occupation…”

What do beekeepers think? What percentage of them accept the assumption that one can grab a bee, attach something to its body, release it, and then expect it to go on its way as if nothing had happened? In my experience, such a bee would fly an escape path and would not likely continue a presumably “programmed” behavior. Those interested in what recruited bees normally might do after leaving the hive, including search for an odor source can access:

http://www.beesource.com/pov/wenner/az1991.htm

That publication of ours contains several quotations by von Frisch that stand in sharp contrast to the observations and claims made in this latest Nature publication.

Some other questions might have occurred by now to beekeepers and bee researchers:

1) What about the very small sample size - can the behavior of 19 disturbed bees undermine the results obtained from hundreds of unrestrained bees searching for odor sources in our double controlled and strong inference experiments? (And, note, only two bees showed up near the target station in the radar tracking experiment after some unspecified time delay.)
2) What about the behavior of the many other bees they must have experimented upon. Did they only gather data from fewer than two dozen bees and then quit when they had supportive evidence?

Tracking recruited bees with radar to study their flight paths after leaving the hive is a noble goal, provided the bees have not been disturbed. Neither do results obtained without the use of odor have relevance to the language hypothesis (as pointed out by Rosin, above). Also, the experimenters should not bother to conduct research unless they can set aside any vested interest in the outcome; that is, that they should instead execute a true test of the language hypothesis and not attempt only to seek confirmation of their prior entrenched beliefs.

As is usual in such a case, some reporters contacted me for my impressions of the Nature report. David Perlman of the San Francisco Chronicle recognized that I had not had time to study the publication and came out with a fairly accurate assessment in his article. Other reporters would not accept my explanation that I would need a few days to study the original publication, with a rather common comment: “I have a deadline to meet.”

No, I don’t think that the behavior of 19 bees will resolve this controversy, one that has run now for well more than three decades. Nor will beekeepers benefit from the claims made in this latest effort. They can go back to worrying about varroa mites, small hive beetles, and other real problems with, hopefully, some real solutions appearing in the near future. Consider the money and time spent on this supposedly final solution to the bee language controversy! Wouldn’t that time and effort have been better spent on breeding a varroa resistant bee, for example?

Despite assertions by the radar tracking crew, the exotic bee language controversy will remain with us for quite some time to come. As stated at the outset, the controversy does not revolve about evidence with respect to validity of the hypothesis. The dance language hypothesis fails to account for all the available evidence with respect to the fundamental question: “How does a naïve bee find a target food source?

Bee language advocates should now address the really important question (how do they find food) instead of attempting to prove a hypothesis. The favored hypothesis continues to be elusive. Until they address the full role of odor as first elucidated by von Frisch, we will continue at a stalemate in the controversy (see: http://www.beesource.com/pov/wenner/jib2002.htm).

In summary, did radar tracking of bee flight paths resolve the bee language controversy? No, it did not; indeed, in the protocol recently reported in Nature, it could not. Because now, just as for the past thirty plus years, a statement that Patrick Wells and I published in Nature back in 1973 (pages 171-175) still holds true “. . . the honey bee forager recruitment controversy is not about the nature of evidence but rather about the nature of hypotheses. It is not what investigators observe (the data) but what they believe (infer) that is at the heart of the controversy.” See: http://www.beesource.com/pov/wenner/natjan1973.htm

Adrian M. Wenner
967 Garcia Road
Santa Barbara CA 93103
wenner@lifesci.ucsb.edu

______________________

ANATOMY OF A CONTROVERSY: THE QUESTION OF A “LANGUAGE” AMONG BEES (Columbia University Press, 1990) pgs: 111-128
______________________

ADRIAN M. WENNER
PATRICK H. WELLS

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“The brain of a bee is the size of a grass seed and is not made for thinking. The actions of bees are mainly governed by instinct. Therefore the student of even so complicated and purposeful an activity as the communication dance must remember that he is dealing with innate patterns, impressed on the nervous system of the insects over the immense reaches of time of their phylogenetic development.”

-Karl von Frisch 1962:78

“Anomalies . . . are the commonest intellectual vehicles for breaking through; all are solvable in the sense that any one is understandable, but that one leads with the power n to still more and deeper anomalies.”

-John Steinbeck (1941) 1962:150

Anomalies encountered during scientific research, although most often ignored due to paradigm hold, at other times provide a basis for solid research. However, even though anomalies are common and valuable during the conduct of research, anomalies and their impact can quickly fade from consciousness as more solid evidence gains priority; what is anomalous under one paradigm becomes the expected after a “conversion” to another paradigm (gestalt switch).

In this and in the following chapter, we include anecdotes from our own experience as examples of the importance of anomaly and how it directed the course of our own research. The recognition of the existence of those anomalies and the consideration of various interpretations led to changes in our subsequent experimental designs. Augmentation of our own experiences by the input of even a single anecdote from other people often helped create new images in our minds.

Edward Jenner’s account of studies of the link between cowpox and smallpox is a significant example of what would now be considered an unacceptable inclusion of anecdotes in a published paper. That research, however, led to the eventual worldwide eradication of smallpox (see excursus JNR). Jenner included a series of anecdotes in order to augment his case, but (as indicated above) a single anecdote may help “create an image” and lead one to new interpretation.

“LEARNING” VERSUS “INSTINCT” AMONG INSECTS

In the 1940s and 1950s only a few students of insect behavior explained behavioral patterns in terms of learning. Most others proceeded strictly within an “instinct” paradigm while interpreting behavioral patterns (see the von Frisch epigraph, above). The “spirit of the times” was permissive; either explanation could be used for a given behavioral act, despite the lack of experimental tests.

Earlier, Loeb ([1918] 1973) and Fraenkel and Gunn ([1940] 1961) had advocated the use of a more quantitative approach to descriptions of animal behavior, including a series of terms that persist today (e.g., “taxes” and “kineses” for animals and “tropisms” for plants). Since 1950, however, the prevailing thought in ethology has shifted gradually toward ever less well-defined terminology and assumptions. The “instinct” versus “learning” issue remains obscure and largely ignored in the animal behavior community (Rosin 1980a, 1980b; see also our chapter 13).

THE “INSTINCTIVE LANGUAGE” OF BEES

Research on honey bee communication during the 1940s and 1950s, then, still relied heavily upon the notion that the behavior of these small animals was largely “innate” or “instinctive” (see the von Frisch epigraph). Thorpe summarized that attitude as follows:

Much of the recent work on insects and other arthropods seems to fit in very well with the hierarchy concept of instinctive behaviour of Tinbergen. Perhaps this fact . . . receives some further elucidation from recent researches on the mode of action of the insect nervous system. Thus Vowles (1961) points out that the properties of the insect neurone, which are very different from that of the vertebrates, and the small size of the insect nervous system, render necessary a functional organisation of behaviour far simpler than is often supposed. (1963:231)

The attitude that insect behavior was fundamentally more simple than that of vertebrates would seem to exclude the possibility of a “language” among bees (Rosin 1978). However, if one pursues research within the verification approach (the Carnap arm of the Realism school), it is possible to retain both notions; a simple system can permit the existence of “language” if one considers the more complex behavior to be merely a fixed sequence of simple steps. Tinbergen verbalized that amalgamation as follows:

When “unemployed” honey bees, waiting in the hive for a messenger, are at last activated by one performing the “honey dance,” . . . the stimulus delivered by the dancer bee stimulates them to leave the hive. They fly in a definite direction over a definite distance (both communicated to them by the dancer) and begin to search for flowers, selecting only those that emanate the scent carried by the messenger. They suck honey [sic], and after having made a “locality study,” they fly home. In this latter case the stimulus given by the messenger [dancing bee] releases a complicated behaviour pattern. (1951:54, 55)

The “chain reflex” explanation of behavior, as used by Tinbergen and others at that time, permitted the phenomenon of honey bee recruitment to food sources to be known eventually as an “instinctual signaling system.” The teleological notion of “purposefulness,” which later came to be so fundamental in ecology and sociobiology, also was relied upon in those early days. Thorpe, for example, invoked that concept in describing honey bee recruitment to food sources, as follows:

An insect with such a high degree of organisation of labour, and having only a limited period of the year in which to forage, needs some means of communication by which a scout which