Honey bees learn and communicate in order to find food sources and for other means.
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Learning is essential for efficient foraging. Honey bees are unlikely to make many repeat visits if a plant provides little in the way of reward. A single forager will visit different flowers in the morning and, if there is sufficient attraction and reward in a particular kind of flower, she will make visits to that type of flower for most of the day, unless the plants stop producing reward or weather conditions change. Honey bees are quite adept at associative learning, and many of the standard phenomena of classical conditioning take the same form in honey bees as they do in the vertebrates that are the more usual subjects of such experiments.
Foragers were trained to enter a simple Y-shaped maze that had been marked at the entrance with a particular color. Inside the maze was a branching point where the bee was required to choose between two paths. One path, which led to the food reward, was marked with the same color that had been used at the entrance to the maze, while the other was marked with a different color. Foragers learned to choose the correct path, and continued to do so when a different kind of marker (black and white stripes oriented in various directions) was substituted for the colored markers. When the experimental conditions were reversed, rewarding bees for choosing the inner passage marked with a symbol that was different from the entrance symbol, the bees again learned to choose the correct path. Extending the length of the tunnel to increase the time between seeing the one marker indicating the correct path and a second marker identifying the correct path show that the bees can retain the information in their visual working memory for about 5 seconds, equivalent to the short-term memory of birds.[1]
One of the most common ways that honey bees, Apis mellifera, demonstrate associative learning is in the context of color recognition and discrimination tasks. Just as vertebrate species such as mice or pigeons that can be trained to perform associative learning tasks, honey bees make excellent subjects for tasks involving discrimination and color memory. Beginning in the early 1900s, scientists Karl von Frisch and later Randolf Menzel began asking questions about the existence, learning rates, memory, and timing of color vision in bees.[2]
The Austrian zoologist Karl von Frisch began the exploration of color vision in honey bees when he asked the first question in 1919: does color vision in bees exist? By making use of bees associative learning abilities he performed an elegant experiment to show that honey bees were in fact capable of color discrimination.[2]
To test color vision, von Frisch first trained his honey bees to feed from a small dish filled with a nectar-like sugar water.[2] This dish was placed over a small piece of blue colored cardboard so that the color was visible to the bees as they fed. Once the bees had become accustomed to the blue cardboard, von Frisch surrounded the blue piece of cardboard with other identically sized pieces in varying shades of gray and placed small dishes over each piece.[3] If bees could not discriminate between colors, they would be unable to distinguish the blue piece from the many gray toned pieces. In the case that bees did not have color vision then, von Frisch predicted that the bees would visit the gray and blue pieces with equal frequency, as they would not be able to tell a difference between them.[2]
When he allowed bees access to the dishes, however, he found that the vast majority of the bees flew directly to the blue piece of cardboard on which they had previously obtained their sugar-water reward.[3] The bees largely ignored the gray pieces which had not been rewarded. This directed exploration and targeting of the blue cardboard showed the bees could indeed discriminate between the gray and blue shades, showing that bees do possess color vision.[3] Von Frisch repeated this same basic experiment to show that bees produced the same results with other colors like red and yellow.[2] Later other researchers were able to apply this excellent experimental design to other vertebrates as well, making it an invaluable insight into testing color vision in many organisms.
After von Frisch’s initial studies, the German scientist Randolf Menzel continued the study of color vision in honey bees and performed more detailed tests. He was curious about which colors honey bees would be able to learn fastest and whether or not bees had a greater aptitude for learning certain colors.
He used lights of varying color and intensity to illuminate circles of light on a solid surface. This set up was similar to the pieces of colored cardboard employed by von Frisch, but by using light instead of cardboard, Menzel was able to change the intensity and color of light easily.[2] He could simply adjust the projection of the light to create a wide variety of different experimental set-ups.
To test the intricacies of the bee color vision von Frisch had established, Menzel performed an experiment that aimed to test bees ability to distinguish between two different colors. To do this, Menzel used a projected circle of colored light surrounding a small dish that could hold a sugar-water reward.[2] Menzel then projected a second circle of differently colored light surrounding a second dish some distance away from the first. Next, a single bee was placed equidistant between these two different lights and allowed to choose which dish to search for a sugar-water treat. Only one of the colored light circles surrounded a dish that contained sugar-water; the other was empty. Menzel was then able to measure how quickly the bees learned to preferentially search only the rewarded light and to ignore the dish surrounded by unrewarded light.[4]
The results of the experiment showed that bees did not learn to discriminate between all color pairs equally well. The fastest rate of learning was when violet light was rewarded.[4] The color that the bees had the most difficulty learning was green, and all other colors fell somewhere in between. This evidence of inherent bias is evolutionarily reasonable given that color vision in bees allows them to distinguish between different nectar-bearing flowers, much like the rewarded dishes.[4] As more flowers are purple than green it makes sense that bees would be more sensitive to colors likely to result in nourishment.[2]
After this work on color preferences, Menzel extended his experiments to study memory in honey bee color vision. He wanted to know how many trials were necessary for honey bees to reliably choose a previously rewarded color when presented with several choices for potential rewards and how long honey bees could retain information about which color would be rewarded.
To test these questions, Menzel performed a variety of experiments. First, he presented individual bees with a sugar reward on a colored background for just a single trial.[4] He then kept these bees in small cages for several days without any further trials. After a few days, he presented each bee with several dishes each on a different colored background at once. One of the colors was the same as that used during the initial trial.[2] The others were novel, unrewarded colors. Amazingly, after just one trial and several days without any exposure to the rewarded color, bees correctly chose to explore the color used in the first trial more than fifty-percent of the time.[4]
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.[4] After several days in confinement when the bees were presented with a choice of colors just as in the first experiment, they virtually always chose the color that had been used during the first three trials.[4]
This ability to retain information about color-linked rewards over a period of several days and after only very minimal exposure to the colored background indicates the great strength of honeybees memory with respect to color vision.
One of von Frisch’s students, Elizabeth Opfinger, observed that bees would learn color when approaching a feeder. Menzel took this question further: when do bees register and learn color? He wanted to know if bees registered color before, during, or after receiving their sugar-water reward. In order to explore this intriguing question, Menzel displayed the color beneath a rewarded dish at different stages of the honey bee feeding process: during approach, feeding and departure.[2]
The outcome of this experiment revealed that bees register color during both the approach and feeding stages of the exposure process.[5] In order for a bee to accurately remember a given color, it must be present for approximately five seconds in total.[5] Although it varies slightly, Menzel and his colleagues found that bees usually remember best when the stimulus is present for about three seconds during the approach and two seconds after landing and beginning to feed.[5]
Color vision in honey bees can also be examined from a neurobiological perspective in terms of the structure and organization of their compound eyes.
In 1975 Menzel published a seminal paper describing the morphology and spectral sensitivity of the honey bee eye.[6] He examined color coding the honey bee retina by using a technique to mark individual cells with a fluorescent dye and record from these cells as single units. Such fine structure analysis allowed him to determine that there are three types of receptors in the honey bee eye: 1) UV receptors, 2) blue receptors, and 3) green receptors.[6] The three receptors are dominated by three rhodopsin-like pigments. These pigments have maximal absorbance at wavelengths corresponding to 350 nm, 440 nm, and 540 nm.[6]
As the cells were examined in detail, certain features were distinguishable for each type of receptor cell. UV cells were found to form the longest visual fibres.[6] These long visual fibers penetrated the lamina with arborizations, a tree-like branching of the fibers and spines. Blue and green receptor cells have more shallow fibers.[6]
Interestingly, Menzel 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.[6] He used spectral efficiency experiments to show that such corresponding wavelength receptivity is the result of electric coupling.[6]
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 language theory is far more widely accepted, and has far more empirical support. The theories also differ in that the former allows for an important role of odor in recruitment (i.e., effective recruitment relies on dance plus odor), while the latter claims that the dance is essentially irrelevant (recruitment relies on odor alone).
It has long been known that successfully foraging Western honey bees perform a dance on their return to the hive, known as waggle dance, indicating that food is farther away, while the round dance is a short version of the waggle dance, indicating that food is nearby. 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. It was thought to attract the attention of other bees.
In 1947, Karl von Frisch correlated the runs and turns of the dance to the distance and direction of the food source from the hive. The orientation of the dance correlates to 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 from the hive. Also, the more vigorous the display is, the better the food. There is no evidence that this form of communication depends on individual learning.
Von Frisch performed a series of experiments to validate his theory.[7] He was awarded the Nobel Prize in Physiology or Medicine in 1973 for his discoveries.
One of the most important lines of evidence on the origin and utility of the dance is 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.[8] 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.
Various experiments document that changes in the conditions under which the dance is performed lead to characteristic changes in recruitment to external resources,[9] in a manner consistent with von Frisch's original conclusions. Researchers have also discovered other forms of honeybee dance communication, such as the tremble dance.
While the majority of researchers believe that bee dances give enough information to locate resources, proponents of the odor plume theory argue that the dance gives 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.
The primary lines of evidence used by the odor plume advocates are
Neither of these points invalidate the dance theory, but simply suggest out that odor might be involved, which is indeed conceded by all proponents of dance theory. Critics of the odor plume theory counter that most natural nectar sources are relatively large - orchards or entire fields. Precision may not be necessary or even desirable. They have also challenged the reproducibility of the odorless source experiment.
Significant to the argument are the elegant experiments of William F. Towne, of the Kutztown University in Pennsylvania, such as this pdf file, in which hives are moved to "mirror image" terrain settings, and thus fooled into both dancing about the wrong location for a nectar source, and successfully recruiting foragers to that wrong location, but only when the sun is obscured by clouds, forcing them to rely on terrain-based navigation rather than "solar ephemeris" based navigation. As the cloud cover breaks up, more and more bees correct their dances to indicate the actual location of nectar, and forager visits shift to the correct location.
The academic debate between these two theories is extremely polarized and often hostile. See here for an overview. Adrian Wenner, a modern bee researcher, is the chief proponent of the odor plume theory (anti-dance). One supporter of Wenner's theories, Julian O'Dea, has proposed an evolutionary explanation for the "waggle dance" that does not involve communication from one bee to another, by claiming it may be a simple idiothetic movement that conveys no information [1]. Conversely, experiments with robotic dummies were indeed able to induce some recruitment,[10] which should not have been possible if the dance contains no information.
An article in the 18 September 2009 issue of New Scientist sets out evidence against the use by bees of the information in the dance [2].
The controversy persists, though it does so primarily due to an asymmetry between the two "camps"; those who study dance communication freely admit that odor is an essential component of the system, and even necessary at various stages of the recruitment process, including once a recruited forager reaches the vicinity of the resource (e.g.[11]), while odor-plume advocates do not acknowledge that the dance contains any information whatsoever. Various experimental results demonstrate that the dance does convey information, but the use of this information may be context-dependent (e.g.[12]), and this may explain why the results of earlier studies were inconsistent. In essence, both sides of the "controversy" agree that odor is used in recruitment to resources, but they differ strongly in opinion as to the information content of the dance.
Odor learning is usually tested by a method called the proboscis extension reflex.
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 [3] though). Other species of Apis use variants on the same theme, and other types of bees use other methods altogether.
The exchange of food, trophallaxis, is also used by means to communicate and includes information on the quality of and thus competition for a food source, temperature and water demand, and the condition of the queen (Sebeok, 1990).
Research that was published in November 2004, by scientists under the leadership of Dr. 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.
Experiments by James Gould suggest that honey bees may have a cognitive map for information they have learned, and utilize it when communicating.
In one test reported in a 1983 issue of Science News, he moved a supply of sugar water 25% further away from a hive each day.[13] The bees communicated to each other as usual on its location. 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, not expecting to find food in the middle of a lake, even though they frequently flew over the lake to reach pollen sources on the opposite shore.
In another test related in the August 1986 issue of Discover ("A Honey of a Question: Are Bees Intelligent?"), Gould lured some bees to a dish of artificial nectar, then gradually moved it farther from the hive after they became accustomed to it. He marked the addicted bees, placed them in a darkened jar, and relocated them to a spot where the hive was still visible, but not the dish. When released one by one, the bees would appear disoriented for a few seconds, then fly directly for the covert dish. Seventy-three of 75 bees reached it in about 28 seconds. They apparently accomplished this feat by devising a new flight path based on a cognitive map of visible landmarks.
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