Bee learning and communication

The honey bee is a well-established model for the study of learning and memory [1]. In a natural context and despite their small size, honeybees exhibit an extremely rich behavioral repertoire. A social lifestyle is obligatory, and a single bee cannot survive very long independent of its mates. Outside of the hive a bee travels over distances of several kilometers and visits hundreds of flowers in a quick and efficient succession for gathering food (nectar and/or pollen). It also collects resin or water, or roams for information-gathering purposes. Sensory capacities and motor performances are highly developed. Bees see the world in color, perceive shapes and patterns and resolve movements with a high temporal resolution. Their olfactory sense is able to distinguish a large range of odors and mechanosensory perception is also extremely rich due to thousands of hair cells all around the body and proprioreceptors inside the body. In a natural context, bees learn and memorize the local cues characterizing the places of interest, which are essentially the hive and the food sources. In the case of food sources, learning and memory are the very basis of floral constancy, a behavior exhibited by foragers which consists in foraging on a unique floral species as long as it offers profitable nectar and/or pollen reward. Only when such an offer becomes unprofitable, bees will switch to a different species. Learning and memorizing the sensory cues of the exploited flower through their association with nectar and/or pollen reward is what allows a bee forager tracking a particular species in the field. Similarly, learning abilities for landmark constellations and for celestial cues used in navigation (azimuthal position of the sun, polarized light pattern of the blue sky) ensure a safe return to the nest and enhance foraging efficiency. Honeybees communicate information about important locations around the hive through ritualized body movements, called the “waggle dance”, a communication system that transmits information about the vector flown toward an attractive food source or nest site. Hive bees attending such a dance decode from the speed of dance movement the distance to the food source and from the angle of the waggling phase relative to gravity the flight direction relative to the sun. In this context, specific associations are built as dance followers learn to associate the odor of nectar brought by a dancer with the nectar that it regurgitates and passes them through trophallactic contacts. Usually, many such dances occur in parallel within a colony. Individual and collective decision-making result from multiple and independent decisions without reference to full knowledge of all potential options available. The complexity and richness of the honeybee’s life is therefore appealing in terms of the opportunities it offers for the study of learning and memory. This study is possible thanks to the existence of controlled laboratory protocols that have been developed to allow experimental access to bee learning and memory .
Experimental access to learning and memory in honeybees
Honeybees can be easily trained individually to solve different kinds of discrimination problems [2]. Various experimental protocols have been implemented to study learning and memory in honeybees at the individual level. Such an individual approach is important because learning and memory result from individual experience and because a neurobiological approach can be then undertaken and correlated with individual learning and memory scores only if such scores have been recorded in a precise way. Three main protocols developed to study honeybee learning and memory can be mentioned here: 1) appetitive conditioning of the approach flight towards a visual target in free-flying bees, 2) appetitive olfactory conditioning of the proboscis extension reflex in harnessed bees, 3) aversive olfactory conditioning of the sting extension reflex in harnessed bees. In the first two protocols, bees are rewarded with sucrose solution as an equivalent of nectar. The third protoocol represents a case of aversive learning as bees learn to associate odorants paired with the noxious reinforcement of an electric shock. In all cases, and with different possible modifications derived from particular experimental needs, the basic experimental design comprises an acquisition or training phase in which the bees experience a particular stimulus or perform a given task that is reinforced, and a test or retention phase without reinforcement in which the bees are presented with the trained situation in order to assess the memory created by training. Eventually, novel stimuli can be presented in the test together with the trained stimulus in order to study generalization and discrimination capabilities. Transfer to novel stimuli (i.e. in absence of the trained stimulus) can also be tested to characterize the flexibility of the bee’s choice (see below).
Conditioning of the approach flight towards a visual target in free-flying bees
Free-flying honeybees can be conditioned to visual stimuli such as colors, shapes and patterns, depth and motion contrast, among others [3]. In such a protocol, each bee is individually marked by means of a color spot on the thorax or the abdomen so that individual performances can be recorded. The marked bee is generally displaced by the experimenter towards the training/test place where it is rewarded with sucrose solution to promote its regular return (Fig. 1a). Such pre-training is performed without presenting the training stimuli in order to avoid uncontrolled learning. When the bee starts visiting the experimental place actively (i.e., without being displaced by the experimenter), the training stimuli are presented and the choice of the appropriate visual target reinforced with sucrose solution. Bees are trained and tested individually to achieve a precise control of the experience of each subject when it enters into a particular test. It is also important to control the distance at which a choice is made because orientation and choice are mediated by different visual cues at different distances or angles subtended by the target. The time between visits to the experimental place is also an important variable to be recorded as it reflects the appetitive motivation of the bee and thus its motivation to learn. For a food source distance of approximately 100 m from the hive, motivated bees take between 2 and 10 min between foraging bouts. Longer intervals may reflect a lower appetitive motivation and thus unreliable data. Several behaviors can be used to quantify the bees’ choice in these experiments. Touches (i.e. the flights towards a target that end with a contact of the bee’s antennae or legs with the stimulus surface) and landings on a given stimulus are usually recorded to this end. The associations built in these context can be either operant, classical or both, i.e. they may link visual stimuli (CS) and reward (US), the response of the animal (e.g. landing) and the US, or both. The experimental framework is nevertheless mainly operant as the bee’s behavior is determinant for obtaining or not the sucrose reinforcement.
Olfactory conditioning of the proboscis extension reflex in harnessed bees
Apart from visual stimuli, honeybees can be conditioned to olfactory stimuli [4]. In such a protocol, each bee is restrained in an individual harness such that it can only freely move its antennae and mouth-parts (mandibles and proboscis). The antennae are the bees’ main chemosensory organs. When the antennae of a hungry bee are touched with sucrose solution, the animal reflexively extends its proboscis to reach out to and suck the sucrose (proboscis extension reflex or PER). Neutral odorants blown to the antennae do not release such a reflex in naive animals. If, however, an odorant is presented immediately before sucrose solution (forward pairing), an association is formed which enables the odorant to release the PER in a following test (Fig. 1b) This effect is clearly associative and constitutes a case of classical conditioning, i.e. the odorant can be viewed as the conditioned stimulus (CS) and the sucrose solution as the rewarding, unconditioned stimulus (US). Within this framework, bees learn to associate the odorant with the sucrose reward. As in any learning protocol, it is important to ensure the appropriate appetitive motivation of the experimental subjects. Immobilized bees in the laboratory have therefore to be starved prior to conditioning. Two to three hours or a whole night are usually used as starvation periods in which bees have to be kept in a calm, darkened, humid environment. In olfactory PER conditioning, the response recorded is the extension of the proboscis which is a dichotomous response (1 or 0). The duration of PER can also be recorded in order to provide a continuous, instead of a discrete, measure of acquisition. To quantify learning, responses to the CS (the odorant) have to be measured before US delivery in each acquisition trial. Quantifying responses to the US is also important to control for the presence of the unconditioned reaction and thus for the maintenance of the appetitive motivation of the bee throughout the experiment. A useful practice is to check the integrity of PER before and after the experiment by touching the antennae with sucrose solution. Animals not exhibiting PER in these control assays should not be included in the experimental analyses as negative responses during acquisition and/or retrieval can be due to sensory-motor deficits instead of learning and/or memory deficits.
Olfactory conditioning of the sting extension reflex in harnessed bees
Contrarily to the previous protocols, this conditioning form offers the opportunity to study aversive instead of appetitive learning in honeybees [5]. In this case, each bee is restrained in an individual harness such that it builds a bridge between two metallic plates through which an electric shock can be delivered (Fig. 1d). Bees stimulated in this way exhibit an unconditioned, defensive reaction which is the extension of the sting (sting extension reflex or SER). Using odorants paired with electric shocks, it is possible to condition the SER so that bees learn to extend their sting in response to the odorants previously punished. Because no appetitive responses are involved in this protocol, true aversive learning can be characterized in this way. As in appetitive olfactory conditioning of PER, the experimenter controls the stimulus contingency and can therefore vary the interstimulus interval and/or the intertrial interval in order to study the impact of these variations on aversive olfactory memory. Responses recorded are also dichotomous (1 or 0) but continuous measures can be obtained by recording SER duration. To quantify learning, responses to the CS (the odorant) have to be measured before shock delivery in each acquisition trial. Quantifying responses to the shock is also important to control for the presence of the unconditioned reaction and thus for the aversive motivation of the bee throughout the experiment. As for PER conditioning, the integrity of SER has to be checked before and after the experiment to ensure the reliability of the data recorded.

Color learning in honeybees
A number of experiments have demonstrated color recognition, discrimination and memory in honey bees Apis mellifera. Beginning in the early 1900s, scientists Karl von Frisch and later Randolf Menzel began asking questions about color vision and various aspects of color learning in bees.[6]
Color discrimination

The Austrian zoologist Karl von Frisch began the exploration of color vision in honey bees when, in 1919, he asked whether or not bees have color vision. He performed an elegant experiment that showed not only that the bees could discriminate colors but that they demonstrated associative learning.[6] He first trained his bees to feed from a small dish filled with a nectar-like sugar water.[6] This dish was placed on a piece of blue colored cardboard so that the color was visible to the bees as they arrived at the dish and fed. Next, von Frisch placed identically sized pieces of cardboard in varying shades of grey, each with a dish, all around the blue piece.[7] Lacking color vision, the bees should visit one or more of the gray pieces as often as the blue piece, but he found the vast majority of the bees flew directly to the blue piece of cardboard on which they had previously obtained their reward.[7] The bees largely ignored the gray pieces which had not been rewarded.[7] Von Frisch repeated the experiment with other colors like violet and yellow and got the same results.[6] Later other researchers used this experimental design to test the color vision of vertebrates.
Color learning rates and preferences
The German scientist Randolf Menzel continued the study of color vision in honey bees with more detailed tests. He was curious about whether bees would learn certain colors faster than others. He used lights of various color and intensity to project circles of light on a surface, a set-up like that used by von Frisch except that, by using light instead of cardboard, Menzel was able to easily change the intensity and color of the circles.[6]

To test bees ability to distinguish between two different colors, Menzel placed a small dish containing sugar-water in one circle and a second empty dish some distance away on a differently colored circle. A single bee was placed equidistant between the two circles and allowed to choose between the dishes. The bees quickly learned to choose the color signaling the dish with the reward, and Menzel was able to measure how quickly the bees learned this task with various color differences.[8]
Menzel's results showed that bees do not learn to discriminate between all color pairs equally well. Bees learned the fastest when violet light was rewarded, and the slowest when the light was green; the other colors fell somewhere in between. This evidence of inherent bias is evolutionarily reasonable, given that bees forage for differently-colored nectar-bearing flowers, many of which are to be found in green foliage which does not signal reward.[6][8]
Color memory
After his work on color preferences, Menzel extended his experiments to study aspects of color learning and memory. He wanted to know how many trials bees need to reliably choose a previously rewarded color when they are presented with several alternatives, and how long they would remember the rewarded color.
Menzel did several experiments to answer these questions. First, he gave individual bees a single sugar reward on a colored background. He then kept these bees in small cages for several days without any further trials. After a few days, he presented each bee with an array of several dishes, each on a different colored background. One of the colors was the same as that used during the initial trial, and the others were novel, unrewarded colors. Remarkably, after a single trial and several days without exposure to the rewarded color, bees correctly chose to explore the color used in the first trial more than fifty-percent of the time.[6][8]
Menzel then repeated this experiment with another group of bees, keeping all factors the same except that in the second round of testing he gave the bees three initial trials with the rewarded color instead of just one. When, after several days in confinement, the bees were presented with a choice of colors they almost always chose the color that was used on the first three trials.[8]
This ability to retain information about color-linked rewards for several days after minimal exposure to the rewarded color demonstrates the remarkable facility with which bees learn and retain color information.
Timing in color learning
In still other experiments, Menzel explored the timing of bee color learning by testing whether bees register color before, during, or after receiving their sugar-water reward. For this purpose Menzel displayed the color beneath a rewarded dish at different stages of the honey bee feeding process: during approach, feeding and departure.[6]
Menzel found that bees register color during both approach and feeding, and that they had to see the color for about a total of about 5 seconds, with best performance usually coming with about three seconds exposure during the approach and two seconds after landing and beginning to feed.[9]
Communication
Foragers communicate their floral findings in order to recruit other worker bees of the hive to forage in the same area. The factors that determine recruiting success are not completely known but probably include evaluations of the quality of nectar and/or pollen brought in.
There are two main hypotheses to explain how foragers recruit other workers—the "waggle dance" or "dance language" theory and the "odor plume" theory. The dance theory is far more widely accepted, and has far more empirical support than the odor theory. Supporters of the dance theory often grant odor a significant role in recruitment, while supporters of the odor theory have claimed that the dance is essentially irrelevant to recruitment. The academic debate between these theories has been polarized and sometimes hostile.[10]
Dance communication

It has long been known that successfully foraging Western honey bees perform a waggle dance upon their return to the hive. The laden forager dances on the comb in a circular pattern, occasionally crossing the circle in a zig-zag or waggle pattern. Aristotle described this behaviour in his Historia Animalium.[11] This waggle pattern of movement was thought to attract the attention of other bees. In 1947,[12] Karl von Frisch correlated the runs and turns of the dance to the distance and direction of the food source from the hive. He reported that the orientation of the dance is correlated with the relative position of the sun to the food source, and the length of the waggle portion of the run is correlated to the distance of the food from the hive. Von Frisch also reported that the more vigorous the display is, the better the food. Von Frish published these and many other observations in his 1967 book The Dance Language and Orientation of Bees[13] and in 1973 he was awarded the Nobel Prize in Physiology or Medicine for his discoveries.
Later work has supported Von Frisch's observations and added many details. It appears that all of the known species and races of honey bees exhibit the behavior, but details of its execution vary among the different species. For example, in Apis florea and Apis andreniformis (the "dwarf honeybees") the dance is performed on the dorsal, horizontal portion of the nest, which is exposed. The runs and dances point directly toward the resource in these species. Each honey bee species has a characteristically different correlation of "waggling" to distance, as well.[14] Such species-specific behavior suggests that this form of communication does not depend on learning but is rather determined genetically. It also suggests how the dance may have evolved.
Other experiments further document the communicative nature of the waggle dance. For example, dances by robotic dummy bees induced some recruitment.[15] Research has also shown that the dance may vary with the environmental context, a finding that may explain why the results of some earlier studies were inconsistent. [16][17]
Odor plume
While many researchers believe that bee dances give enough information to locate resources, proponents of the odor plume theory argue that the dance gives little, or no actual guidance to a nectar source. They argue that bees instead are primarily recruited by odor. The purpose of the dance is simply to gain attention to the returning worker bee so she can share the odor of the nectar with other workers who will then follow the odor trail to the source. Most scientists agree that odor is used in recruitment to resources, but they differ strongly in opinion as to the information content of the dance.[citation needed]
The primary lines of evidence used by the odor plume advocates are
- experiments with odorless sugar sources which show that worker bees are unable to recruit to those sources[18] and
- logical difficulties of a small-scale dance (a few centimeters across) giving directions precise enough to hold the other bees on course during a flight that could be several kilometers long. Misreading by even a few degrees would lead the bee off course by hundreds of meters at the far end. [citation needed]
Neither of these points invalidate the dance theory, but simply suggest that odor might be involved, which is indeed conceded by all proponents of dance theory.[citation needed] Critics of the odor plume theory counter that most natural nectar sources are relatively large—orchards or entire fields— so, precision may not be necessary or even desirable. They have also challenged the reproducibility of the odorless source experiment.
Odor learning in bees is usually tested by the proboscis extension reflex. Significant to the argument are the experiments of William F. Towne, of the Kutztown University in Pennsylvania,[19] in which hives are moved to "mirror image" terrain settings, and the bees are thereby fooled into dancing about the wrong location for a nectar source. Foragers were successfully recruited to the wrong location, but only when the sun was obscured by clouds, forcing them to rely on terrain-based navigation rather than "solar ephemeris"-based navigation. As the cloud cover broke up, more and more bees corrected their dances to indicate the actual location of nectar, and forager visits shifted to the correct location.
Odor is essential and even necessary at various stages of the recruitment process, including once a recruited forager reaches the vicinity of the resource[20] while some scientists think that dancing may be a simple idiothetic movement that conveys no information.[21] Others see the dance as conveying information, but doing it poorly compared to other means and potentially used backup approach.[22]
Note: much of the research on the two competing hypotheses of communication has been restricted to Western honey bees (see the work of F.C. Dyer[23] though). Other species of Apis use variants on the same theme, and other types of bees use other methods altogether.
Trophallaxis
The exchange of food, trophallaxis, can be used to communicate the quality of a food source, temperature, a need for water, and the condition of the queen (Sebeok, 1990).
Primer pheromones
Research that was published in November 2004, by scientists under the leadership of Zachary Huang, Michigan State University indicates that so called primer pheromones play an important part in how a honey bee colony adjusts its distribution of labor most beneficially. In order to survive as a bee colony of sometimes 50,000–100,000 individual bees, the communal structure has to be adaptable to seasonal changes and the availability of food. The division of labor has to adjust itself to the resources available from foraging. While the division of labor in a bee colony is quite complex, the work can be roughly seen as work inside the hive and outside the hive. Younger bees play a role inside the hive while older bees play a role outside the hive mostly as foragers. Huang's team found that forager bees gather and carry a chemical called ethyl oleate in the stomach. The forager bees feed this primer pheromone to the worker bees, and the chemical keeps them in a nurse bee state. The pheromone prevents the nurse bees from maturing too early to become forager bees. As forager bees die off, less of the ethyl oleate is available and nurse bees more quickly mature to become foragers. It appears that this control system is an example of decentralized decision making in the bee colony.
Other bees like Trigona corvina rely on pheromones for much of their communication with nest mates and rivals.[24] They produce pheromones from their labial glands.[25] The function of signaling depends on the profitability, but they commonly will scent mark a food source either for self-orientation, to deter rivals or to direct a nest mate to the resource. Once an individual finds a good food source, they will return to the same source for many days. If an individual detects the scent of a rival bee, they will avoid the plant in order to avoid conflict and to save time.[24] It has also been shown that pheromones are a method of sexual selection between male drones and queens.[25]
Cognition
Experiments by James Gould suggest that honey bees may have a cognitive map for information they have learned, and utilize it when foraging. In an experimental demonstration,[26] Gould lured some bees to a dish of artificial nectar, then gradually moved it farther from the hive. He marked the trained bees, placed them in a darkened jar, and relocated them to a spot where the dish could not be seen but the hive was still visible. When released one by one, the bees appeared disoriented for a few seconds, then flew directly to the dish, 73 of 75 bees reaching it in about 28 seconds. They apparently accomplished this feat by devising a new flight path based on a cognitive map of visible landmarks.
Another test suggested not only the use of a map, but also an ability to remember and combine relevant information. Gould moved a supply of sugar water 25% further away from a hive each day. The bees communicated the location of the water to each other as usual. Then he placed the sugar water on a boat anchored in the middle of a small lake. When scouts returned to the hive to communicate their find, other bees refused to go with them, even though they frequently flew over the lake to reach pollen sources on the opposite shore. To Gould these observations suggested that "bees somehow consider information to see if it makes sense before they act on it".[27]
Neurobiology of color vision

A seminal paper by Menzel (1975) described the morphology and spectral sensitivity of the honey bee eye that underlie their color vision.[28] He examined color-coding in the honey bee retina by marking individual cells with a fluorescent dye and recording from these cells as single units. From this analysis he determined that there are three types of receptors in the honey bee eye: 1) UV receptors, 2) blue receptors, and 3) green receptors The three receptors contain three rhodopsin-like pigments which have maximal absorbance at wavelengths of 350 nm, 440 nm, and 540 nm. Menzel also found that most of the cells he studied had secondary sensitivities that corresponded to wavelength regions at which the other two receptor types were maximally active. He used spectral efficiency experiments to suggest that these secondary sensitivities result from electric coupling between the receptors.[28]
Certain morphologies distinguished the receptor types. UV cells were found to have long visual nerve fibers that penetrated the lamina with deep tree-like branchings. Blue and green receptor cells had more shallow fibers.[28]
See also
- Bumblebee communication
- Eusociality
- Grooming dance
- Trained hymenoptera
- Tremble dance
- Waggle dance
- Zoosemiotics
References
- ^ Giurfa, M. (July 17, 2007). "Behavioral and Neural Analysis of Associative Learning in the Honeybee: A Taste From the Magic Well". J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 193 (8): 801–824. doi:10.1007/s00359-007-0235-9. PMID 17639413.
- ^ Giurfa, M. (July 17, 2007). "Behavioral and Neural Analysis of Associative Learning in the Honeybee: A Taste From the Magic Well". J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 193 (8): 801–824. doi:10.1007/s00359-007-0235-9. PMID 17639413.
- ^ Avarguès-Weber, A.; Deisig, N.; Giurfa, M. (2011). "Visual Cognition in Social Insects". Annu Rev Entomol. 56: 423–443. doi:10.1146/annurev-ento-120709-144855. PMID 20868283.
- ^ Bitterman, M.E.; Menzel, R.; Fietz, A.; Schäfer, S. (1983). "Classical conditioning of proboscis extension in honeybees (Apis mellifera)". J Comp Psychol. 97: 107–119. PMID 6872507.
- ^ Vergoz, V.; Roussel, E.; Sandoz, J.C.; Giurfa, M. (2007). "Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex". PLoS One. 2(3): e288. doi:10.1371/journal.pone.0000288.
{{cite journal}}
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- ^ a b c Frisch, K. von. 1956. Bees; their vision, chemical senses, and language. Ithaca, N.Y., Cornell University Press.
- ^ a b c d Menzel, R. and Backhaus, W. 1989. Color vision in honey bees: Phenomena and physiological mechanisms. In D. Stavenga and R. Hardie (eds): Facets of vision. Berlin-Heidelberg-New York: 281-297
- ^ Menzel, R. and Backhaus, W. 1991. Colour Vision in Insects. In P. Gouras (ed): Vision and Visual Dysfunction. The Perception of Colour. London: MacMillan Press, 262-288.
- ^ Munz, T. (November 2005). "The Bee Battles: Karl von Frisch, Adrian Wenner and the Honey Bee Dance Language Controversy". Journal of the History of Biology. 38 (3): 535–570. doi:10.1007/s10739-005-0552-1.
- ^ "HISTORIA ANIMALIUM". virginia.edu.
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- ^ von Frisch, K. (1967) The Dance Language and Orientation of Bees. Cambridge, MA: Harvard Univ. Press.
- ^ Dyer, F.C.; Seeley, T.D. (1991). "Dance dialects and foraging range in three Asian honey bee species". Behavioral Ecology and Sociobiology. 28 (4): 227–233. doi:10.1007/bf00175094.
- ^ Michelsen, A.; Anderson, B. B.; Kirchner, W. H.; Lindauer, M. (1989). "Honeybees can be recruited by a mechanical model of a dancing bee". Naturwissenschaften. 76 (6): 277–280. Bibcode:1989NW.....76..277M. doi:10.1007/BF00368642.
- ^ Visscher, P.K. and Tanner, D.A. (2004). Sensory aspects of recruitment-dance performance in honey bees (Apis mellifera). in: Hartfelder, K.H, De Jong, D. et al. eds. (2004) Proceedings of the 8th IBRA International Conference on Tropical Bees and VI Encontro sobre Abelhas. Ribierao Preto: USP/FM
- ^ Sherman, G.; Visscher, P.K. (2002). "Honeybee colonies achieve fitness through dancing". Nature. 419 (6910): 920–922. Bibcode:2002Natur.419..920S. doi:10.1038/nature01127. PMID 12410309.
- ^ "Experiments on Directing Bee Flight by Odors". beesource.com.
- ^ http://faculty.kutztown.edu/towne/Towne_2008_JEB_211_3737-3743.pdf
- ^ Riley, J.R.; Greggers, U.; Smith, A.D.; Reynolds, D.R.; Menzel, R. (2005). "The flight paths of honeybees recruited by the waggle dance". Nature. 435 (7039): 205–207. Bibcode:2005Natur.435..205R. doi:10.1038/nature03526. PMID 15889092.
- ^ "Why do honeybees dance?". beekeeping.com.
- ^ Williams, Caroline (18 September 2009). "Rethinking the bee's waggle dance". New Scientist (2726). Archived from the original on 2009-09-23. (subscription required)
- ^ Publications of Fred C. Dyer. Archived September 14, 2006, at the Wayback Machine
- ^ a b Neeltje Janna Boogert; Frouke Elisabeth Hofstede; Ingrid Aguilar Monge (2006). "The use of food source scent marks by the stingless bee Trigona corvina (Hymenoptera: Apidae): the importance of the depositor's identity". Apidologie. 37 (3): 366–375. doi:10.1051/apido:2006001.
- ^ a b Jarau, Stefan; Dambacher, Jochen; Twele, Robert; Aguilar, Ingrid; Francke, Wittko; Ayasse, Manfred (2010-09-01). "The Trail Pheromone of a Stingless Bee, Trigona corvina (Hymenoptera, Apidae, Meliponini), Varies between Populations". Chemical Senses. 35 (7): 593–601. doi:10.1093/chemse/bjq057. ISSN 0379-864X. PMID 20534775.
- ^ Gould, J L "A honey of a question, are bees intelligent?" Discover, 1986, August
- ^ Miller, J A "Biology" Science News; 4/23/1983, Vol. 123 Issue 17, p271, 1/6p
- ^ a b c Menzel, R; Blakers, M (1975). "Colour receptors in the bee eye — Morphology and spectral sensitivity". Journal of Comparative Physiology A. 108: 11–13. doi:10.1007/bf00625437.
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- Leoncini I, Le Conte Y, Costagliola G, Plettner E, Toth AL, Wang M, Huang Z, Becard JM, Crauser D, Slessor KN, Robinson GE (December 14, 2004). "Regulation of behavioral maturation by a primer pheromone produced by adult worker honey bees". Proceedings of the National Academy of Sciences of the United States of America. 101 (50): 17559–64. Bibcode:2004PNAS..10117559L. doi:10.1073/pnas.0407652101. PMC 536028. PMID 15572455.
- Miller, Julie Ann (April 23, 1983). "Do Bees Plan Ahead Intelligently?". Science News. 123 (17). Society for Science &: 271. doi:10.2307/3967590. JSTOR 3967590.
- Sebeok (1990). Essays in Zoosemiotics. Toronto: Toronto Semiotic Circle. ISSN 0838-5858 .
External links
- Honeybee Communication
- Genetic Control of the Honey Bee (apis mellifera) Dance Language: Segregating Dance Forms in a Backcrossed Colony
a very detailed introduction to the honey bee dance language. (.pdf file). - Paper by Adrian Wenner: https://web.archive.org/web/20031203211713/http://beesource.com/pov/wenner/jib2002.htm
- Martin tomato, et al.: The concepts of 'sameness' and 'difference' in an insect, Nature, 410, 930-933 (19 April 2001)
- The Sensory Basis of the Honeybee's Dance Language, W Kirchner & W Towne, Scientific American
- Jacqui Hayes: Pleasure chemical controls bee dance COSMOS magazine