ABOVE: Bock's pygmy octopus (Octopus bocki) in experimental tank Robyn Crook

Back in 2008, the bees in Lars Chittka’s honey bee (Apis mellifera) laboratory at Queens University of London started behaving as if they were seeing ghosts. In the Chittka lab, bees are housed together in dark, artificial nests meant to mimic the conditions of the natural cavities where they typically build their hives. For behavioral experiments, the insects are usually transferred via a long tube one by one into small arenas where they learn to perform complex tasks such as counting and classifying objects into distinct categories.

In Chittka’s study, bees foraged in a meadow of yellow and white artificial flowers—hand-sized squares where they would encounter a sucrose-filled syringe. There was a chance that when they approached a flower, however, they would be briefly caught by a soft, mechanical claw made of foam. This brief interaction mimicked capture by one of the bees’ natural predators: crab spiders (Misumena vatia). While the “capture” lasted for only two seconds, for a day afterward the bees learned not just to avoid flowers harboring predators, but approached all flowers more cautiously, signaling that they still, in some sense, remembered their temporary capture. “The bees were overall more nervous,” Chittka says. “To us, it appeared as if there was something emotional going on, beyond just aversive learning.”

Yellow spider camoflaged on yellow flower
A crab spider (Misumena vatia) camouflaged on a yellow flower, waiting for its prey.

Decades ago, scientists and lawmakers had all but reached a consensus that invertebrates could not feel pain, let alone other emotions like joy or fear. Recently, however, evidence is mounting that invertebrates are more than just reflexive beings. Experiments in bees, crabs, and octopuses show that some invertebrate animals can learn from painful experiences, have positive and negative emotion-like states, and might even experience a range of other emotions beyond pain and pleasure. But not all scientists agree that invertebrates feel anything analogous to vertebrate—much less human—emotion.

Frans de Waal, a primatologist and animal behaviorist at Emory University, and Kristin Andrews, a philosopher at the University of York, make the case for invertebrate emotion in a March paper published in Science. The evidence that invertebrates can learn and experience things beyond just simple reflexes, the duo argues, is now “overwhelming.” And if invertebrates indeed have emotions, they add, it may change the way we relate to and treat them, making them a part of our moral landscape. Still, many scientists remain extremely skeptical, and the question of whether invertebrates can experience emotions is hotly debated. 

Challenging dogma

Up until the 1980s, doctors still performed some surgeries on infants with little or no anesthesia. The practice persisted because of infants’ inability to tell doctors what they felt, and the perception that they wouldn’t remember the pain. By and large, animals’ pain was dismissed for similar reasons. 

In the early 20th century, behaviorism, which deemphasized internal experiences, was the prevailing method of conducting cognitive science, says de Waal. “As a consequence, the field of [animal emotion] is new. It's certainly new to science, even though every dog owner that you meet will talk about the emotions of his or her dog.”

Most emotion researchers now agree that human infants and other vertebrate animals, especially primates, have emotions, but distinguish emotions from feelingsFeelings are internal states that are subjective and therefore impossible to measure, they agree. “The principal difficulty that we face with all animals is that . . . we don’t have access to what they feel or think through verbal reports,” says Chittka. Emotions are different. 

“Emotions are states that prepare the organism for action, usually an adaptive action that is necessary for survival. Fear is the most obvious one,” de Waal says. Emotions elicit a physiological response that can be measured—a change in blood pressure, breathing, body temperature, facial expression, or body posture—that readies an animal to make a decision. Emotions are thought to have a cognitive component, as well as behavioral and physical ones. 

Orangutan looking fed up
Primates such as orangutans (Pongo pygmaeus) show emotions on their faces.
© iStock.com, Freder

Studying emotions in nonhuman primates is the simplest, due to their similarity to humans, says de Waal, who has long studied chimpanzees (Pan troglodytes). Primates display facial expressions that are similar to ours, furrowing their brows in a seeming display of frustration, baring their teeth to display rage, and smiling, perhaps to express something akin to joy. Common laboratory mice (Mus musculus) also seem to change their facial expressions to express emotions, and their physiological and neurological responses to pain, anxiety, and social defeat are well-documented.

With animals that are more evolutionarily distant from humans, measuring emotional states becomes trickier, says de Waal. Most invertebrates, for example, can’t vocalize or express emotions on their faces—if they even have something akin to a face. Invertebrate nervous systems, physiology, and sensory experiences are dissimilar to ours, and designing experiments to measure their emotions has been challenging. 

De Waal posits that deep-seated assumptions have been another barrier to studying invertebrate emotions. “You can see that bees can get agitated, so they must have emotional states. But no one really talked about it, and no one took it seriously,” he says. That’s now beginning to change, both for bees and for other invertebrates.

“When I was a PhD student in the 90s, people would never have taken seriously the idea that bees might have emotion-like states. People would have laughed,” Chittka says. 

Considering lobsters

While at a pub in the 1990s, crustacean researcher Robert Elwood, now an emeritus neuroscientist at Queen’s University Belfast, met popular UK seafood chef Rick Stein. Stein, upon learning that Elwood studied crustaceans, asked him if lobsters feel pain. The same question had been considered by philosophers, writers, and scientists for years. As David Foster Wallace observed in his famous essay “Consider the Lobster,” crustaceans are the only animals we still kill—in slow deaths, by boiling and steaming, no less—in kitchens.

“I thought, ‘that’s a very silly question, because you can’t get an answer,’” Elwood recalls. But Elwood’s curiosity was piqued, and after he parted ways with Stein, the scientist started to seriously think about how he would go about answering the chef’s question.

Person holding up lobster claws up
For some, whether lobsters feel pain as they're boiled alive remains an open question.
© iStock.com, Philip Rozensk

At the time, many scientists had accepted that vertebrates, at least, could feel pain. This pain went beyond a reflexive aversion—or nociception—akin to automatically jerking your hand back from a hot stove. Most scientists now agree that pain is a complicated emotional and physical state. “Pain is by definition, both a physical and an emotional experience,” says Robyn Crook, a pain researcher and neurophysiologist at San Francisco State University who studies cephalopods. “It has to be the . . . sensation of something noxious into the central nervous system, but also the higher cognitive processing associated with that sensation that creates . . . an emotional response, which is what we characterize as pain.”

But most scientists in the 1990s were convinced that invertebrates can’t feel pain, Elwood says. Instead, scientists hypothesized that insects, fish, and crabs relied solely on instinct to avoid injury during their relatively short lifespans. As late as 2010, the official ruling of the Canadian Senate was that invertebrates couldn’t feel pain, based on findings in insects. This was accepted dogma because some insects indeed behave like they don't feel anything at all. Locusts continue to chew leaves as they’re being consumed by predators, and many insects don’t limp in response to injury.

“It was thought that they can’t possibly experience pain, because all their responses are purely by reflex,” Elwood says. “I thought, . . . it should be possible to ask, ‘are the responses reflexive or not?’” If the responses weren’t purely reflexive, it would open up the possibility that the animals could feel pain. 

Starting in the late 2000s, Elwood began testing whether crustaceans feel pain. Elwood began by working with shore crabs (Carcinus maenas), asking whether the crabs groomed or rubbed a putatively painful area. After placing acetic acid—a mild irritant—on the crabs’ antennae, they found that the crabs rubbed their antennae against the glass of their aquarium, seemingly in an attempt to take the acid off. The response was reversible with the application of an anesthetic, a dynamic Elwood says is “consistent with the idea of pain.” The crabs also seemed to be able to learn and change their behavior in response to electric shocks, indicating that their processing of the shock was more than a reflex reaction.

Tank with rocks on the bottom and two shelters
Arena with two dark shelters where crabs would get shocks on one side and not the other
Barry Magee

In nature, shore crabs hide under rocks during low tide, as they are likely to be killed and eaten by predators when out in the open. In another experiment, Elwood built a brightly-lit, open enclosure filled with shallow water and placed two dark, crab-sized shelters on either side. When the researchers placed the crabs in the middle of the tank, the crabs immediately ran to one of the shelters, showing a preference for one side upon repeated trials of the task. But when they began receiving electrical shocks in their preferred shelter, they changed their preference, showing that they might be able to experience and learn from painful stimuli, Elwood says. “It seemed to be consistent with the idea of pain . . . the function of pain seems to be to provide long term protection.” 

“The fact that they remember these locations means that they have experienced pain,” de Waals argues.

In subsequent experiments, Elwood showed that the crabs have stress responses after electrical shocks, and that hermit crabs (Pagurus bernhardus) also changed their preferences in response to shocks, choosing to leave their shells after receiving painful stimuli, but only if the odor of a predator was not present. 

The idea that invertebrates feel pain has been met with deep skepticism by other researchers, who argue that they still find the evidence for pain in crustaceans to be thin. 

Karen Mesce, a neuroscientist at the University of Minnesota, points out that crustaceans—like insects—lack the nervous system structures that allow humans and vertebrates to feel pain. In humans, pain and fear are processed in the amygdala and the limbic cortex, which the brains of crustaceans and insects lack. Human brains “have these special structures so that we can recall a heightened sense of whether things are good and bad,” she says.  

Mesce argues that insects don’t need an emotion-like state, or even a brain, to learn to avoid painful stimuli. She notes that in a study where researchers shocked the legs of headless cockroaches inside a saline bath, the insect bodies “learned” to keep their legs lifted outside of the water. And most would argue that a headless cockroach isn’t experiencing an emotional-like state, Mesce says. 

David Merrit, an entomologist at the University of Queensland in Australia who coauthored a key review on invertebrate pain in 1984 that argued against the existence of pain in insects, agrees. Insects—and their close evolutionary cousins, crustaceans—can learn to avoid noxious stimuli, he says, but it seems unlikely that crabs and insects are experiencing something analogous to human pain when they receive a shock. 

“Think about an electrical shock stimulus. When we’re shocked it goes straight to our pain center, overriding our senses. But it’s a stretch to say that [invertebrates are] feeling pain the way that we feel pain,” Merrit says. “The word ‘feeling’ is a human thing. We think we can ascribe it to animals or insects, but we really can’t.”

But de Waal argues that the ability to process and remember their surroundings suggests the existence of an internal state, which further suggests that invertebrates have emotion-like capabilities. “If you learn from . . . good or bad experiences, you must have experiences, which means that you have feelings” about a situation, he says. “So if I shock you, and you learn from that, that means you must have experienced pain. Otherwise, why would you memorize the situation? Memory . . . means that you have experiences.”

Super smart cephalopods 

While there is not a clear consensus on the existence of pain in insects, more researchers seem to be on board with the idea that cephalopods have the capacity to feel pain.

Crook, who also researches pain in mammals, says she was curious about pain and its relationships to the fundamental organizing principles of animal minds, so she started researching pain in brainier invertebrates—cephalopods—including Bock's pygmy octopus (Octopus bocki). “I got interested in looking at where in the animal kingdom you find pain and why. Is pain an exclusively human/mammalian thing or is it more widespread?”

See “What Scientists Learned by Putting Octopuses in MRI Machines

A common method to study pain in rodents is the conditioned place preference (CPP) test, which assesses an animal’s ability to remember and learn which side of an environment it received a shock. As marine animals, octopuses move and explore their environment in a fundamentally different way than mammals, meaning Crook had to adapt the behavioral assay to fit their needs. It “was no easy task,” says Crook, which is likely why such experiments hadn’t been done before.

Crook designed a tank with two visually distinct sides, one with stripes and one with dots. After a single training session in the tank, an octopus would form a preference for one side or the other. Then, Crook and her team anesthetized the octopus and injected dilute acetic acid into one of its tentacles, which Crook describes as the equivalent of a “bit of lemon juice in a cut.” As the octopus woke up, presumably with a tentacle aching quite a bit, the researchers confined it to the side of the chamber it preferred less. When the acid dissipated about 20 minutes after the injection, the octopus was taken out, then added back in five hours later. Crook and her colleagues observed which side of the tank the octopus chose to spend its time in, finding that the animals avoided the side where they had been confined when they received the acidic treatment. The task is cognitively demanding, says Crook. It requires the octopus to remember where it was and ascribe a negative valence to that location—thus, perhaps, feeling some way about it.

Octopus vulgaris in conditioned place preference tank
Octopus bocki in a conditioned place preference tank
Robyn Crook

“The interpretation is that [the octopus] is choosing based on its evaluation of its mental or affective state, that it remembers from a previous experience,” Crook says. The finding was hailed as the best evidence of invertebrate emotion so far. Crook says it demonstrates that pain and therefore emotion evolved in parallel along different branches of the evolutionary tree and are not just restricted to mammals. She adds that she hopes scientists can move beyond asking if octopuses feel pain and address questions about their welfare. 

“I thought that [Crook’s] paper was wonderful,” says Shelly Adamo, a neuroscientist at Dalhousie University in Nova Scotia, Canada, who has worked with insects, crustaceans, and cephalopods throughout her career. Adamo says that in her view it’s unlikely that insects feel pain, given that “Insects and crustacea have what’s called a distributed nervous system. They have many brains throughout their body, [which] reduces the information processing power.” In contrast, “cephalopods [have] taken those mini-brains and, just like us, squeezed them all into a big main brain.” Therefore, she says, it’s more likely that cephalopods are able to feel pain than are other invertebrates, and the paper is “good evidence that [pain] could be there.”

“It was nice to see, and I think it’s a study that kind of gets beyond the reasonable doubt,” Crook says. “But it’s very hard to convince people who are on the fence or are clearly not believers in invertebrate emotion.”

Pain points

Mesce, Adamo, and Merritt all question whether invertebrates, with their relatively simple nervous systems, have the processing power to feel emotions. They also question why invertebrates would even need emotions. With so few neurons (lobsters have about 1 million, while humans have about 86 billion), Adamo argues, devoting any energy to emotions might be wasteful. “As you [look] into animals that have smaller and smaller brains, they may be very selective about which capacities they have. It may be that [animals with smaller brains] may only have some type of emotions that are a faint echo of what we would recognize as an emotion.”

Andrews says that this is a common argument—that while the physiological components, like an increase in heart rate after seeing a snake, are clearly useful, the felt aspect is unnecessary for invertebrates. One could argue, Andrews says, that the felt aspect of emotion is equally unnecessary for vertebrates. Artificial intelligences and robots, for example, don’t have emotions such as pain, but can act as if they do. But the simplest explanation for the felt aspect of emotion, Andrews argues, is that emotions have some sort of evolutionary significance. “If something doesn’t have a function it can’t evolve, right? [Emotion’s] function is to learn . . . why else would I go toward something . . . if I didn’t have a positive emotion associated toward that thing?” 

“For most animals, the pain is a way the animal is interpreting the tissue damage or whatever is being done. And that very unpleasant feeling makes learning so much easier,” Elwood agrees.

Looking beyond pain

Some evidence suggests it may be possible for smaller animals with even tinier nervous systems and brains to feel not just pain, but more complicated emotions akin to optimism and pessimism. Chittka had been observing as bees learned amazingly complex feats for years when he stumbled on a paper positing that bees have pessimistic cognitive biases. In the study, researchers placed bees in a vorticizer, an instrument used to mix liquids. After vigorously shaking the bees, then scientists then exposed the insects to an ambiguous stimulus, a mix of an odor associated with a reward and another associated with a bitter-tasting substance. Much like when humans are depressed, he says, the shaken bees appeared to judge the ambiguous substance as negative, becoming more reluctant to investigate the mixed scent.

Negative and positive cognitive biases are complicated emotional states often used to gauge animals’ wellbeing, says Chittka. Intrigued by the experiment, he decided to do a similar one, this time testing whether bees could also have positive cognitive biases. In his experiment, an individual bee climbed into a flight chamber via a metal tube. The bee climbed into one end to see two target squares—one blue and one green—on the other end. Below the colored square was a small cylinder that the bee had to climb through to potentially receive a reward. Below the blue target, the bee received a sugar water reward. But below the green one, the bee received quinine, a sugar that, while not toxic, is bitter and aversive to the insects.

Honey bee caught by crab spider on top of pink flower
Honey bee (Apis mellifera) caught by crab spider
Lars Chittka

After some training, when bees saw a blue target, they rushed to the reward within seconds. But when they saw the green target, they took significantly longer to land on that square. 

In a subsequent experiment, Chittka gave some of the trained bees a droplet of sugar water before they entered the chamber. Others received sugarless water. He then presented the bees with an ambiguous stimulus: a greenish-blue square. This time, to Chittka’s surprise, the bees that had received sugar water tended to travel to the cylinder much faster, an indication that they might have been anticipating a reward.

In humans, “someone who is optimistic and not depressed will more likely judge an ambiguous situation like that as being potentially a good thing,” Chittka says. 

The researchers’ interpretation of the finding was that the bees that received sugar entered a positive affective state, perhaps akin to optimism, and were biased to perceive the ambiguous stimulus as positive. The team also found that if they blocked dopamine, a signal associated with reward and learning in mammals, the sugar reward had no effect. 

See “Dopamine Drives Bee Desires: Study

“It is surprising. We’re dealing with animals whose brain is the size of a pinhead with just about a million neurons,” says Chittka. “I think what we have to recognize is that invertebrates are not like rocks—that they’re individuals we share our planet with.”

Still, Merritt argues that emotions in bees are a far cry from anything akin to emotions in humans. “Now, they might have some sort of neural state that we could equate with an emotion. . . . but to then take all the baggage we’ve associated with humans and put it on insects and other invertebrates—I think it’s an error,” he says. He adds that he doubts that the findings are applicable to other insect species, which still might act purely on instinct.

Ethical implications of invertebrate pain

Despite the fact researchers can’t agree on whether invertebrates feel emotion or not, some legislators have been convinced of the possibility. In 2013, the UK, which has some of the strictest animal protections in the world, added cephalopods to its list of protected animals under the Animals in Scientific Procedures Act (ASPA), which regulates how animals are used in research. These types of protections are also getting extended to other invertebrates. In 2018, Switzerland outlawed the practice of boiling lobsters alive. According to The GuardianElwood’s research played a role in this decision. And in late 2021, the UK passed a law that recognizes some invertebrates, including crabs and lobsters, as sentient. The decision was based on a report commissioned by the government and compiled by the London School of Economics (LSE), which created a framework of eight criteria for determining whether decapod crustaceans, such as crabs and lobsters, could experience pain, distress, or harm (including the presence of nociceptors, integrated brain regions, and whether analgesia can head off pain responses). The law mandates that UK ministers consider the sentience of animals when implementing new animal welfare policies. While the law has had no immediate effects on animal welfare in the UK, it could result in future restrictions on how lobsters and crabs are treated in research settings. Animal welfare laws vary widely by country, however, and in the US, such laws only cover certain vertebrates in the context of breeding, lab research, and animal cruelty.

Recognizing pain in invertebrates, Andrews says, could or perhaps should affect the way humans interact with such animals. Most humans don’t want to cause any animal unnecessary amounts of pain. But the specifics of what to do once we know an animal feels pain—if animal husbandry or research practices should change, for example—are up for debate. Even regarding vertebrates, “these are all tricky ethical questions,” Andrews says.

Octopus in corner of tank
Octopus bocki
Robyn Crook

As more evidence stacks up that invertebrates are able to experience something akin to emotion, it could prompt further changes in animal welfare laws that widely affect how animals are used in animal research or for consumption. 

Crook and Andrews say that invertebrate emotion-like states may be very different from human emotions, but perhaps it is worth understanding why invertebrates have emotion-like states in and of themselves. “When we’re talking about ‘what does an animal feel,’ in some ways, you’re asking, what is it acceptable to do to that animal, right? So it’s often approached from a very utilitarian . . . anthropocentric, human supremacist viewpoint, and not necessarily about the broader evolutionary lives of animals,” Crook says.

“I think it’s easier for people to say, ‘Oh, my dog has emotions,’ but harder for people to recognize emotions in a crab, for instance. It’s a very automatic response,” Andrews says. “But then you have to be careful of anthropomorphizing and making sure you’re not just projecting your own feelings” onto the animal. Interrogating our relationships to animals, and how animals’ emotions relate to ours, she says, “is the beginning of the research, not the end.”