One balmy autumn day in 2014, David Reynolds stood up to speak at an important meeting. It was taking place in Chicago City Hall – a venue so grand, it's embellished with marble stairways, 75ft (23m) classical columns, and vaulted ceilings.
As the person in charge of pest management in the city's public buildings, among other things, Reynolds was there to discuss his annual budget. But soon after he began, an imposter appeared on one of the walls – a plump cockroach, with her glistening black body contrasting impressively with the white paint. As she brazenly sauntered along, it was as if she was mocking him.
"Commissioner, what is your annual budget for cockroach abatement?" one councillor interrupted, according to a report in The Chicago Tribune. Cue raucous laughter and a mad scramble to eradicate the six-legged prankster.
No one would question the cockroach's impeccable, though accidental, comic timing. But the incident is partly funny because we think of insects as robotic, with barely more emotional depth than lumps of rock. A cockroach that's capable of being amused or playful – well, that's just plain absurd. Or is it?
In fact, there's mounting evidence that insects can experience a remarkable range of feelings. They can be literally buzzing with delight at pleasant surprises, or sink into depression when bad things happen that are out of their control. They can be optimistic, cynical, or frightened, and respond to pain just like any mammal would. And though no one has yet identified a nostalgic mosquito, mortified ant, or sardonic cockroach, the apparent complexity of their feelings is growing every year.
When Scott Waddell, professor of neurobiology at the University of Oxford, first started working on emotions in fruit flies, he had a favourite running joke – "…that, you know, I wasn't intending on studying ambition", he says.
Fast-forward to today, and the concept of go-getting insects is not so outrageous as it once was. Waddell points out that some research has found that fruit flies do pay attention to what their peers are doing, and are able to learn from them. Meanwhile, the UK government recently recognised that their close evolutionary cousins – crabs and lobsters – as sentient, and proposed legislation that would ban people from boiling them alive.
So, how does one detect emotions in an insect? How can we tell they're not just responding automatically? And if they really are sensitive creatures, should we treat them differently?
For insects, golden tortoise beetles are unusually good at making their feelings clear (Credit: Alamy)
An evolutionary imperative
Insects are a jumbled group of six-legged invertebrate creatures with segmented bodies. There are more than a million different types, encompassing dragonflies, moths, weevils, bees, crickets, silverfish, praying mantis, mayflies, butterflies, and even head lice.
The earliest insects emerged at least 400 million years ago, long before dinosaurs took their first tentative plods. It's thought our last common ancestor with them was a slug-like creature which lived around 200 million years before that, and they've been diversifying ever since. Initially they ruled over the land as giants – some dragonflies were sparrowhawk-sized, with 2.3ft (70cm) wingspans – before evolving into the extraordinary array of arthropods around today, from flies with fake scorpion tails to fuzzy moths that resemble winged poodles.
As a result, they're strikingly similar to other animals, and yet vividly different. Insects have many of the same organs as humans – with hearts, brains, intestines and ovaries or testicles – but lack lungs and stomachs. And instead of being hooked up to a network of blood vessels, the contents of their bodies float in a kind of soup, which delivers food and carries away waste. The whole lot is then encased in a hard shell, the exoskeleton, which is made of chitin, the same material fungi use to build their bodies.
The architecture of their brains follows a similar pattern. Insects don't have the exact same brain regions as vertebrates, but they do have areas that perform similar functions. For example, most learning and memory in insects relies on "mushroom bodies" – domed brain regions which have been compared to the cortex, the folded outer layer that's largely responsible for human intelligence, including thought and consciousness.
(Tantalisingly, even insect larvae have mushroom bodies, and some of the neurons within them remain for their whole lives – so it's been suggested that adult insects that went through this stage might be able to remember some things that happened before they metamorphosed.)
There's mounting evidence that our parallel neural setups power a number of shared cognitive abilities, too. Bees can count up to four. Cockroaches have rich social lives, and form tribes that stick together and communicate. Ants can even pioneer new tools – they can select suitable objects from their environment and apply them to a task they're trying to complete, like using sponges to carry honey back to their nest.
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However, though insect brains have evolved down an uncannily familiar path to our own, there is one crucial difference: while human ones are so engorged they sap 20% of our energy and drove women to evolve wider hips, insects have compacted their wits into packages several million times smaller – fruit flies have brains the size of a poppy seed. How they've managed this is an enduring scientific mystery to this day.
Asian honeybees scream with their bodies, by vibrating them (Credit: Alamy)
So, even at first glance, it seems like insects would have the intellectual capacity for emotions. But does it make sense that they would have evolved them?
Emotions are mental sensations that are usually linked to an animal's circumstances – they're a kind of mental programme that, when it's set off, can change the way we act. It's thought that different emotions have emerged at different points in evolutionary history, but broadly they turned up to encourage us to behave in ways that will improve our ability to survive or reproduce, and ultimately, maximise our genetic legacy.
Geraldine Wright, a professor of entomology at the University of Oxford, gives the example of hunger, which is a state of mind that helps you to alter your decision-making in a way that's appropriate, such as prioritising food-seeking behaviours. Other emotions can be equally motivating – rumblings of anger can focus our efforts on rectifying injustices, and constantly chasing happiness and contentment nudges us towards achievements that keep us alive.
All these things could also apply to insects. An earwig that's thrilled when it finds a nice damp crevice filled with delectable rotting vegetation will be less likely to starve or dry out, just as one that panics and plays dead when it's disturbed has a better chance of escaping the jaws of a predator.
"Let's say you're a bee that ends up in a spider web, and a spider is swiftly coming towards your across the web," says Lars Chittka, who leads a research group that studies bee cognition at Queen Mary, University of London. "It's not impossible that the escape responses are all triggered without any kind of emotions. But on the other hand, I find it hard to believe that this would happen without some form of fear," he says.
A heretical idea
When Waddell first started his own research group in 2001, he had a fairly simple goal in mind. He wanted to find out if flies are better at recalling where to find food when they haven't eaten for a while – i.e. when they might, if they could experience subjective moods, be feeling "hungry". (It turns out they are, and they can.)
It's difficult to study pain in fruit flies because they don't respond to morphine. However, they are partial to cocaine (Credit: Alamy)
To begin with, Waddell cautiously chose the word "motivation", rather than "hunger", to describe the flies' state of mind – he suggested that they were more motivated to find food if it had been withheld. "And people found it a little problematic," says Waddell. Some other scientists felt that this was too anthropomorphic and preferred the term "internal states". "So I often had arguments that I thought were essentially meaningless, because they were just playing with that word," he says.
Then in a matter of years, studying insect intelligence became significantly more fashionable – and all of a sudden the term "motivation" was abandoned, with researchers making the case for insects having "emotional primitives", says Waddell. In other words, they experienced what looked suspiciously like emotions.
"I had always thought of these physiological changes that occur when animals are in deprivation states – deprived of sex, deprived of food – as subjective feelings of 'hunger' and 'sex drive'," says Waddell. "I've never really bothered labelling them as 'emotions', pretty much because I thought it was going to get me into trouble. But before I knew it, everyone seemed to be more comfortable using that [word]."
Now that the suggestion insects have feelings is slightly less scandalous, the field has exploded in popularity – and this strange group of animals is becoming more relatable by the day. But proving that an insect can experience an emotion remains tricky.
Take the humble bumblebee.
In humans, those who have experienced trauma are especially wired to expect the worst – and this has also been demonstrated in a number of other vertebrate animals, including rats, sheep, dogs, cows, cod and starlings. But no one had ever thought to check if insects did this too.
Back in 2011, together with colleagues from Newcastle University (where she worked at the time), Wright decided to take a look. "When psychologists are studying this in humans… they can verify affect [a person's emotional state] because they can ask," says Wright. But discerning emotions in bees requires a bit more ingenuity.
Cockroaches are highly sociable and copy the behaviour of their peers, just like humans do (Credit: Alamy)
First, the researchers trained a troupe of bees to associate one kind of smell with a sugary reward, and another with an unpleasant liquid spiked with quinine, the chemical that gives tonic water its bitter taste. Then the scientists divided their bee participants into two groups. One was vigorously shaken – a sensation bees hate, though it's not actually harmful – to simulate an attack by a predator. The other bee crowd was just left to enjoy their sugary drink.
To find out if these experiences had affected the bees' mood, next Wright exposed them to brand new, ambiguous smells. Those who had had a lovely day usually extended their mouthparts in expectation of receiving another snack, suggesting that they were expecting more of the same. But the bees who had been annoyed were less likely to react this way – they had become cynical.
Intriguingly, the experiment also hinted that the bees weren't experiencing some alien, unrelatable form of pessimism, but a feeling that might not be too dissimilar to our own. Just like humans who are feeling exasperated, their brains had lower levels of dopamine and serotonin. (They also had lower levels of the insect hormone octopamine, which is thought to be involved in reward pathways.)
Wright says many of the chemicals in our brains are highly conserved – they were invented hundreds of millions of years ago. So an insect's emotional experiences could be more familiar than you would think. "So from that perspective, yes, they [the brain chemicals] may have diverged a little bit in terms of what they signal in which animal lineage, but it's quite interesting," she says.
For example, Waddell's research on fruit flies has found that their brains use dopamine just like ours do, to elicit feelings of reward and punishment. "So it's very, very interesting that those things have, you know, convergently evolved and are sort of similar," says Wright. "It means that that's the best way of doing it."
Wright explains that her bee experiment doesn't necessarily mean that all insects can experience pessimism or optimism, because bees are unusually social – community life at the hive is particularly cognitively demanding, so they're considered intelligent for insects. "…But other insects probably do [have pessimism] too," she says.
A clear message
However, it would be surprising if insects could feel emotions but not express them at all. And tantalisingly, there are some hints that insects might be more relatable than you'd think here too.
Industrial farming has turned much of the earth's surface into a hostile environment for insects (Credit: Alamy)
The problem is something Charles Darwin first considered in the late 19th Century. When he wasn't pondering evolution or eating the "strange flesh" of the exotic fauna he discovered, he spent much of his time thinking about how animals communicate their feelings, and wrote up his findings in a little-known book.
In The Expression of the Emotions in Man and Animals, Darwin argues that – just like every other characteristic – the ways humans express their feelings would hardly have appeared out of nowhere in our own species. Instead, our facial expressions, actions and noises are likely to have evolved via a gradual process over millennia. Crucially, this means that there's probably some continuity among animals, in terms of the ways that we display our emotional state to others.
For example, Darwin noted that animals often make loud noises when they're excited. Among the loud chattering of storks and the threatening rattling of some snakes, he cites the "stridulations", or loud vibrations, of many insects, which they make when they're sexually aroused. Darwin also observed that bees change their hums when they're cross. This all suggests that you don't need to have a voice box to express how you're feeling.
Take the golden tortoise beetle, which looks like a miniature tortoise that's been dipped in molten gold. It's not actually covered in the element, but instead achieves its glamorous look by reflecting light off fluid-filled grooves embedded in its shell. However, pick one of these living jewels up – or stress it out in any way – and it will transform before your eyes, flushing ruby-red until it resembles a large iridescent ladybird.
Most research on the beetle has focused on the physics of how it achieves the colour switch, but intriguingly, it's thought that the response is controlled by the insect, which may choose to change depending on what's going on around it – rather than something that just happens passively.
Insects have diversified to fill almost every conceivable niche, but they all share similar brains – so emotions in insects may be universal (Credit: Alamy)
Then there's the Asian honey bee. Around October each year – during what's ominously referred to as the "slaughter phase" – they run the gauntlet of gangs of bee-decapitating giant hornets, also aptly known as "murder hornets". The wasps have a wide native range in Asia, from India to Japan, but scientists suspect they're slowly invading other areas, with occasional sightings in North America. Their raids on bee hives can last for hours, and wipe out entire colonies – first, they cut up their worker bee victims into pieces, then they go for their offspring.
But the bees don't go quietly. In work released earlier this year, scientists revealed that they scream – using an amplified, frantic version of their usual buzz. And though no one has conclusively tied the shrieks to an emotional response in the bees, the study's authors noted in their paper that these "antipredator pipes" share similar acoustic features to the alarm calls of many other animals, from primates to birds to meercats, and might suggest that they're fearful.
An uncomfortable truth
However, the most contentious aspect of the inner lives of insects has to be pain.
"There's lots of evidence in fruit fly larvae that they feel mechanical pain – if we pinch them, they try to escape – and the same is the case for adult flies as well," says Greg Neely, a professor of functional genomics at the University of Sydney. As always, proving that these unpleasant experiences are interpreted as emotional pain is another matter. "The issue is really the higher order aspect," says Neely.
However, there's emerging evidence that they can indeed feel pain as we know it – and not only that, they can experience it chronically, just like humans.
One basic clue to the former is that, if you train fruit flies to associate a certain smell with something unpleasant, they will simply run away whenever you present them with it. "They link together the sensory context with the negative stimulus, and they don't want that – and so they go away from it," says Neely. When fruit flies are prevented from escaping, they eventually give up and exhibit helpless behaviour that looks a lot like depression.
But perhaps the most surprising results have emerged from Neely's own research, which has found that injured fruit flies can experience lingering pain, long after their physical wounds have healed. "It's almost like an anxiety-like state, where once they've been injured, they want to make sure nothing else bad happens," says Neely. The fruit flies' responses are thought to mirror what can happen in humans, when an injury leads to chronic "neuropathic" pain.
Insect populations are declining accross the whole planet (Credit: Alamy)
And though pain hasn’t yet been studied in a wide variety of insects, Neely thinks its likely that it would be similar across the board.
"If we look at the overall architecture of how the brain is set up – the receptors, the ion channels and the neurotransmitters are all pretty similar," says Neely, who points out that you can find examples of insects that are blind to these sensory signals, such as larvae that are in the middle of their transition to adulthood, but this is unusual.
A question of numbers
All this research has some unsettling implications. At the moment, insects are among the most persecuted animals on the planet, routinely killed in almost-incomprehensibly large numbers. This includes 3.5 quadrillion – 3,500,000,000,000,000 – poisoned by insecticides on US farmland each year, two trillion squashed or slammed by cars on Dutch roads, and many more that have gone uncounted.
But though there isn’t much data on the full extent of our insecticide, one thing is widely accepted – the numbers we're despatching are so vast, we're living through an "insect Armageddon", an era where insects are vanishing from the wild at an alarming rate. Three-quarters of the flying insects in German nature reserves have disappeared in the last 25 years, and one report found that 400,000 species may be facing extinction.
During "slaughter season" gangs of giant Asian hornets launch ferocious attacks on honeybees, decapitating the adults and eating their offspring (Credit: Alamy)
The discovery of insect emotions also poses a slightly awkward dilemma for researchers – especially those who have devoted their careers to uncovering them.
Fruit flies are the archetypal research animal, studied so intensively that researchers know more about them than almost any other. At the time of writing, there are around 762,000 scientific papers that mention its Latin name, "Drosophila melanogaster", on Google scholar. Equally, studies into bees are growing in popularity, for the insights they can provide into everything from epigenetics – the study of how the environment can influence the way our genes are expressed – to learning and memory. Both have endured more than their fair share of experimentation.
"I like to watch bees and I've studied behaviour for a lot of my career, so I empathise quite a lot with them already," says Wright, who has been a vegetarian for decades. However, the numbers used in research are tiny compared to those sacrificed elsewhere, so she feels that it’s easier to justify. "It's this sort of disregard of life in general that we have [that Wright finds more problematic] – you know, people just wantonly take life and destroy it and manipulate it … from humans to mammals, insects to plants."
But while using insects for research is still largely uncontroversial, the discovery that they may think and feel raises a number of sticky conundrums for other fields.
There's already a historical precedent for banning pesticides to protect certain insects – such as the EU-wide embargo on nicotinoids for the sake of bees. Could there be scope for moving away from others? And though insects are increasingly promoted as a noble and environmentally friendly alternative to meat from vertebrates, is this actually an ethical win? After all, you'd have to kill 975,225 grasshoppers to get the same volume of meat as you would from a single cow.
Perhaps one reason we don't tend to think of insects as emotional is that it would be overwhelming.
Zaria Gorvett is a senior journalist for BBC Future and tweets @ZariaGorvett
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