The Bee School: Genes and Social Learning in Bees

The Bee School

By JULIETTE IRMER (text) and LANDO HASS (photos)

May 10, 2023 · Whether a honey bee becomes a collector, undertaker or explorer is not just a question of its genes. Personality and talent also play a role.

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alerie Kuklovsky is a bee whisperer. When the biologist places honey solution near a hive, the buzzing and whirring begins within a very short time. "For bees, the honey solution is like the ice cream of the best ice cream parlour," says the doctoral student.

PhD student Valerie Kuklovsky works exclusively with particularly industrious worker bees and is investigating, among other things, how good their long-term memory is.

She has marked the first honey bee at the feeding station with a pink spot between its wings and is now watching what happens. The bee flies back to the hive and does not dance the famous tail dance inside, but runs around in narrow circles and changes the direction of rotation from time to time. The round dance is always used when the food source is close to the stick. The more productive the food source, the livelier the dance. Through feeler contact, other foragers in the hive pick up the smell of the food source and set off in search. They learn from the first discoverer the way to the ice cream counter and quickly set off there. And indeed: After a few minutes, more bees make their way over the "ice".

The experiment, which Valerie Kuklovsky is carrying out at the University of Würzburg, is part of a large project that explores the cleverness and learning ability of insects. After all, the days when they were considered pure reflex machines are long gone. Today it is clear that bees are amazingly capable of learning and that they can even learn from each other. And recently it has also become clear that bees are differently gifted – and this diversity has an evolutionary meaning.

Bees are provided with marking points on their backs to make it easier to find them in the tangle of the colony. Number 78 in this case is the queen bee.

Bees are provided with marking points on their backs to make it easier to find them in the tangle of the colony. Number 78 in this case is the queen bee.

Culture is something that people like to see as a unique selling point of their kind. After all, the animal kingdom lacks baroque churches, paintings, bestsellers and hit parades. At its core, however, culture means that the members of a community cultivate certain behaviors that are adopted by the next generation. In this sense, culture is also found in animals: chimpanzee groups use different tools to crack nuts, orca families pass on unique hunting techniques, and blue in southern England were first observed a hundred years ago picking open the foil lids of milk bottles to get their hands on the cream – a tradition that spread as far as Scotland over time. What all these animals have in common is that they are considered to be extremely intelligent.

A honey bee marked with a pink dot on its back (left) ingests sugar water from a feeding site with its proboscis. The insect was trained by Valerie Kuklovsky on this feeding site. The second, unmarked bee, has learned from the first bee where the sugar water is located.

The circle of cultural workers also includes socially living bees. They impress with an enormous variety of behaviors, build architecturally complex, air-conditioned nests, and the family groups of mother and daughters share the work in their people in a remarkable way. Above all, the honey bee is particularly good at "educating", i.e. learning.

A recent Japanese study in Science Advances shows that new cognitive abilities of the bee are associated with the further development of certain types of nerve cells in the mushroom body, i.e. the part of the insect brain that is responsible for learning. This learning can take place in two ways: the animals can learn individually, or they can learn socially, that is, they observe conspecifics and imitate them, a prerequisite for the development of culture.

Ricarda Scheiner heads the bee station at the University of Würzburg. Together with her team, she is researching how bees learn.

Ricarda Scheiner is also working on the topic of learning ability. The biologist heads the bee station at the University of Würzburg, a garden-like site of around 3000 square meters with many flowering fruit trees. As soon as the sun peeks out from behind the clouds on this cool April day, the hustle and bustle and buzz in front of the excursion hole of the many colorful beehives increases.

More than fifty bee colonies of different sizes live on the site and serve science. Two heated free-flight rooms allow field experiments all year round. "For energy reasons, we are currently doing without it in the winter months," says Scheiner.

This is also where Valerie Kuklovsky's bee ice cream parlor is located. She only uses diligent nectar collecting bees for her learning attempts. For her doctoral thesis, she investigated whether the animals learn consistently, i.e. whether the learning performance of individual bees remains constant or varies on three consecutive days. The result is surprising: there are consistently "smart" and consistently "stupid" bees.

"In the past, you tested a bee ten times and then said n = 10, i.e. sample number equals ten, because you simply assumed that all bees were the same," says Kuklovsky. Yet they have quite different personalities. "After a while, I recognize my test bees from a distance of five meters, even without markings. The way they fly and the way they behave." Some bees are curious, some are afraid.

The more mixed a colony is, the better the division of labor of the bees works.

The tasks that Kuklovsky's protégés solve over several hours are impressive: On gray turntables, she hangs several color plates that differ only slightly in color. The bee is supposed to learn that the yellow shade A offers a reward in the form of sugar water, while the yellow shade B is punished with quinine, a well-known bitter substance. The color plates hang close to each other and change position when the biologist turns the disc. Kuklovsky observes only one bee per day, which receives around 20 approaches per experiment and voluntarily participates, not least because the insect was rewarded with sugar water at the beginning of the experiment series. This first attempt is easy for most bees. Bees must also be able to distinguish flower colours in the wild and reliably recognise those flowers that contain a particularly large amount of nectar.

The second attempt is more difficult, because now suddenly yellow shade B is rewarded with sugar water. "This is quite a challenge, because the bees have to erase the memory trace of the preliminary experiment and relearn," explains Kuklovsky. And it gets even trickier: In "negative patterning", the bees learn to associate a pink-gray checkerboard pattern and a blue-gray checkerboard pattern with sugar water. However, when it comes to the "composite" stimulus, i.e. a pink and blue checkerboard pattern, they come away empty-handed. "That's really difficult, because if A and B are good, AB should be twice as good," Kuklovsky says. The evaluation shows that some bees find it easier to solve the tasks, and their hit rate is almost 100 percent after a while over the three days of the experiment. Other bees, on the other hand, like to participate, but perform worse. There is a kind of normal distribution, that is, "there are few bees that don't understand anything and few bees that learn perfectly".

The so-called associative learning works not only with visual stimuli, but also with scents, which also play a major role in the life of a bee: To demonstrate this, Kuklovsky has carefully fixed four bees in a tube, only the heads can move them freely. With a small syringe containing a piece of filter paper drizzled with scents, she blows on the bees, which immediately stick out their tongues: they have previously learned to connect the scent stream with a spoonful of sugar water. "Some learn it after three times, some never."

However, bees that perform well in visual learning do not automatically perform well in smell – olfactory learning. So, the insects, it seems, have different talents.

"Individual differences in the perception of stimuli are an important factor for the successful functioning of a bee colony," says Scheiner. This is because the division of labour, the highly organised coexistence of the approximately 40,000 bees in the hive, is also associated with different stimulus thresholds. "It works just like in a shared apartment. The person with the lowest stimulus threshold for dirty dishes is the first to start washing," says Scheiner. One bee can be particularly sensitive to the smell of dying conspecifics and then becomes an undertaker bee, another is sensitive to the smell of the brood and then quickly becomes a pollen collector who enters the important proteins for the larval food into the hive. "The more mixed my colony is, the better the division of labor between the bees works, because the stimulus thresholds differ more strongly."

Locked in small tubes, honey bees are trained with sugar solution and puffs of air.

The different stimulus thresholds of the workers and also their cognitive abilities are presumably mainly due to different fathers – the drones. The extent of their role can be seen when a queen is mated with only one drone: A bee colony with only one father is more unstable overall, performs worse in terms of honey yield, and the bees also learn worse than bees from colonies with up to twenty fathers.

Kuklovsky and Scheiner believe that bees with different talents also provide benefits to the colony. For example, it is known from other studies that scouts, i.e. bees looking for new food sources, are particularly capable of learning. "My hypothesis is that there is an even finer division of tasks among forager bees than is previously known," says Kuklovsky, which could explain the different performance of the foragers in the visual tests.

But it is not only individual learning that plays an important role in the hive – social learning as well. A well-studied example of how knowledge is passed on in these insects is the tail dance, for the deciphering of which Karl von Frisch was honored with the Nobel Prize fifty years ago.

A trained bee is released from the tube.

For example, if a forager bee has discovered a blossoming apple tree, it transmits its coordinates with the help of a dance in the hive that is performed in the shape of a figure eight. She wiggles her abdomen energetically. The dances encode the distance, the direction of the compass and even the quality of a food source. "Some colleagues say that there are elements of real language because the bees communicate about something they can't see," says Scheiner.

Like many of the sophisticated behaviors of social insects, dance language is considered innate. And there is no doubt that there is a genetic basis. Only honey bees use this form of communication. The information content is largely programmed, so new meanings that go beyond location and quality are not added.

In a recent research paper in Science, a team led by biologists Shihao Dong of the Chinese Academy of Sciences and James Nieh of the University of California report that performing the tail dance correctly requires social learning in addition to genetic parts. If, as was long believed, the tail dance were completely innate, young bees would perform the dance correctly even if they had never seen the behavior before. For their experiments, the biologists created honey bee colonies consisting exclusively of newly hatched bees. These started the tail dance at the typical age of one to two weeks after hatching, but made significant mistakes in terms of distance and direction of the food source. With increasing experience of the bees, the direction information improved, but they overestimated the distance to the food source throughout their lives.

If, as was long believed, the tail dance were completely innate, young bees would perform the dance correctly even if they had never seen the behavior before.

Young bees that grew up in mixed-aged, normal colonies and were therefore allowed to attend the "dance school", i.e. learned from experienced forager bees, did not make these beginner's mistakes. The authors of the study conclude that social learning decisively shapes the signaling of honey bees, as is also the case with the early communication of many vertebrates. "There are many examples of innate learning behavior that needs to be perfected through social learning," Scheiner confirms. Many songbirds, for example, only learned to sing flawlessly if they were allowed to listen to a living tutor, usually their own father.

Honey bees are pets. Beekeepers keep a colony in each hive, which grows larger and larger as the spring progresses. In autumn and winter, young bees do not hatch, the size of the hive decreases.

In 2020, a study involving Scheiner's colleagues from the Chair of Animal Ecology and Tropical Biology at the University of Würzburg showed that closely related bee species living in the same area dance for different lengths of time to indicate the same distance. These different dance dialects are an adaptation to different sizes of bee gathering areas – and in principle the beginning of culture. "You can certainly argue about the term culture in connection with social insects," says Scheiner, who prefers to speak of cultural transmission, "one thing is certain, relative to its brain size, the bee is a very clever animal."

The sister shows the way

By JULIETTE IRMER

May 10, 2023 · Bumblebees do not pass on what they have learned to their offspring. Are there still behavioral traditions?

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Not only honey bees, but also bumblebees, which also belong to the large family of bees, are capable of astonishing learning achievements. By observing conspecifics, they learn which flower colour promises the most nectar and pollen, and also copy non-natural behaviours such as pulling on a string in order to get a reward when a bumblebee sister shows them how to do it.

Now, a team led by Lars Chittka from Queen Mary University of London has presented another remarkable bumblebee study in the journal Plos Biology. The biologists report that bumblebees learn new behaviors quickly and that they spread rapidly in a bumblebee community through social learning, i.e. observing conspecifics. With these abilities, bumblebees also approach those animals to which humans grant a kind of culture. Well-known examples are the use of tools in primates and corvids.

Finding out how insects gain and pass on knowledge is not trivial. The researchers therefore used the so-called open diffusion paradigm. This is an experimental design that has already been used to test chimpanzees and great and is considered the gold standard within behavioral biology: individual animals are first taught a new technique, then released back into their original community, and biologists document whether and how quickly other group members adopt the new technology.

Chittka's team designed a two-option food box for the bumblebee study, whose attractant, a 50 percent sugar solution, is highly sought after by all bees. The transparent lid of the round Petri dish can be rotated a bit clockwise with the help of a red tab or a blue tab counterclockwise, releasing the treat.

In a first experiment, the researchers taught a single, particularly curious bumblebee step by step to press its head against the red tab of the apparatus in order to get the reward. They placed this so-called demonstrator bumblebee in a closed flying arena that was directly connected to the bumblebee colony.

The bumblebees now had three hours a day for six days to occupy themselves with the food boxes and were filmed in the meantime. At the beginning they showed no interest in the round containers, but by the end of the experiment almost all bumblebees had learned to open the box in the same way as they had been demonstrated, i.e. by pressing against the red tab. Some bumblebees discovered that the box could also be opened when they ran head first against the blue tab, but in the end the animals preferred the variant with the red tab. The researchers repeated the experiment with a bumblebee that they had taught to press against the blue tab. The result was clear: after six days, almost all of the nestmates had learned to press the blue tab.

In the control groups without a demonstrator bumblebee, only one bumblebee spontaneously learned how to open the box. A second round of experiments, which ran for twelve days, also produced a few spontaneous learners, but all of them opened fewer boxes than the trained bumblebees, who opened an average of 28 boxes per day. A high-flyer bumblebee from the control group managed to open 216 boxes in 12 days.

"I was surprised at how flexible and innovative the behaviour of bumblebees really is," says first author Alice Bridges, "the fact that some have learned to open the boxes themselves is remarkable and suggests that bumblebees are capable of dealing with new behaviours." Overall, more than 98 percent of the bumblebees adopted the opening trick they had copied from their nestmates and kept it. According to the researchers, this shows that behaviors in bumblebee groups spread through social learning.

"The similarities between our results in bumblebees and those in primates and birds identified using similar paradigms are remarkable, as these previous studies sought to demonstrate the ability of these species to culture," the study authors wrote.

Whether bumblebees can naturally develop similar behavioral traditions, however, remains an open question. The lifespan of the bumblebee species used in the experiment, the bumblebee Bombus terrestris, which is also common in this country and is also used specifically to pollinate tomatoes and strawberries, is short, only the queen survives and hibernates. It is true that a bumblebee colony, like all other bee colonies, always consists of overlapping generations, because new workers hatch again and again. But if no worker bees survive the end of summer, all traditions of foraging will probably be lost with them. "However, the results reported here support the assumption that the cognitive abilities are available for this."

"Honey bees, stingless bees, and some tropical bumblebees form colonies that last for many years," Bridges says, "if a naturally occurring, long-lived culture were found in an invertebrate species, it would probably be there."

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