Bumblebee facial movements give clues to their inner lives

Bees seem to show when they are pleased and like something, rather than just needing it, in one of the strongest signs yet that insects have subjective experiences.

In recent decades, it has become clear that bees are capable of more complex behaviours than we previously thought, such as counting and demonstrating a sense of rhythm. But discerning whether they have inner states akin to our emotions is more difficult. For one thing, insects don’t have the flexible facial musculature of mammals, which we use to communicate our feelings.

“How can we get any behavioural readout of these insects with a hard body and their mask of a face,” asks Andrew Barron at Macquarie University in Sydney, Australia. “Do bees have any sort of inner state whatsoever?”

To solve the mystery, Barron and his colleagues ran a series of experiments involving buff-tailed bumblebees (Bombus terrestris).

First, the team offered the bees a water droplet containing sugar, along with others that contained salt and quinine, while filming them using high-resolution video.

After tasting the sweet liquid, the bees repeatedly stuck out their glossa, which is a hairy tongue that they use to lap up nectar in flowers. After tasting the salty and bitter samples, the bees wiped their mouths and shook their heads.

However, both responses may have just been a reaction to the different chemicals, rather than a sign of enjoyment or displeasure, says Barron.

Next, the researchers reduced the concentration of the sugar and mixed it with a small amount of salt, resulting in a dramatic reduction of the glossa protrusions. Then they exposed the bees to 40°C (104°F) temperatures to dehydrate them, after which, when the bees were offered salty droplets, the bees repeatedly protruded their glossa.

“If I just handed you an electrolyte drink right now, you’d probably think, ‘well, that actually tastes pretty foul’,” says Barron. “But if you had just come back from a long run and I handed you an electrolyte drink, you’d think, ‘that’s fantastic’. It’s because your internal state has changed, and that internal state is changing your evaluation of things – that’s what we think we’re seeing in the bees.”

For the final part of their experiment, the researchers wanted to determine what would happen if they meddled with the chemistry that, in mammals, underpins appetite and the enjoyment of food.

When the bumblebees were treated with dopamine, which in mammals affects the motivation to seek food, their glossa protrusions didn’t increase, suggesting that although they had greater desire, their enjoyment “tell” – tongue protrusions – didn’t change.

But when the bees were treated with endocannabinoids, which increases the “liking” of food in mammals, it led to an increase in their glossa protrusions.

“What this is showing us is that even from an animal like a bee, there is some sort of inner life for that insect,” says Barron. “There’s something going on. It’s evaluating its world. It’s experiencing its world and it’s not a robotic entity running on a program.”

Ralph Adolphs at the California Institute of Technology says the research is “an important and innovative study on a difficult topic”. “The evidence presented in the paper shows that the bees represent the value of the taste stimuli in a flexible manner,” he says. But it is unclear whether the experiments demonstrate pleasure as we know it.

“The idea that facial expressions are literally constitutive of emotions is clearly not the case. Actors can fake them, and people whose faces are paralysed still have emotions,” he says. “I think we should conclude that bees have bee emotions, not mammal emotions.”

Jonathan Birch at the London School of Economics says the study is the first time he has  seen “wanting” and “liking” disentangled in a bee.

“We underestimate insects so much,” he says. “It’s led to a golden age of very charming studies where scientists use modern techniques – sometimes just high-resolution, high-frame-rate video, as in this study – to reveal behaviours people have been missing.”