Part of our weekly "In Focus" series—stepping back, looking closer.
Chefs have been grappling with the question for years: What's the best way to humanely kill a lobster?
Some cooks recommend tucking the invertebrate into the freezer for an hour, while others prefer quickly stabbing it behind the eyes. For the serious seafood gourmand, there are even stun devices that are advertised as the only way to humanely kill your joint-legged dinner.
All of this hand-wringing and contradictory advice raises a basic, but as yet unresolved question. Can lobsters and other creatures most of us know as seafood actually feel pain?
The scientific debate on the subject has intensified recently, with a team of British researchers proposing this month that electroshock tests suggest crabs indeed feel pain. But the study has drawn scrutiny, while another study late last year pushed back on the idea that fish, more closely related to humans than are crabs, feel pain.
"About six years ago there began a flood of papers that had me thinking that fish may feel pain," says Carleton University's Steve Cooke, who co-authored the paper, titled "Can Fish Really Feel Pain?" "However, when I looked at them closely it was apparent that there were deficiencies."
Competing theories about whether our seafood feels pain points to a broader reality: We know relatively little about the diversity of adverse reactions across the tree of life. Sometimes, even species closely related to those used in a lab test don't react the same way.
While a 2007 study of the prawn Palaemon elegans reported that the crustaceans showed reactions consistent with feeling pain, for instance, attempts to replicate the experiment with the closely related white shrimp and Louisiana red swamp crayfish did not achieve the same results.
Could that be because of truly different sense abilities, a flaw in the experiment, or something else?
Plus, the whole concept of "pain" is squishy.
Asking whether or not a fish on a line or the crab tumbling into the steamer feels pain is akin to asking if those animals can also feel pleasure or contentment. It's difficult to understand the way a shrimp or tuna feels the world around it, especially given our evolutionary distance from them.
The human lineage parted ways with the arthropods, including the ancestors of crabs, over 540 million years ago. Our fishy ancestors, which were more like lungfish and coelacanths than carp or tuna, split from the rest of the piscine family over 420 million years ago.
Yet the way a fish struggles when hooked, and the hard-shelled cringe of a lobster dropped into a boiling pot, suggest that they truly do feel something. Feeling for an answer to this mystery tests the limits of our ability to envision the internal lives of other species.
But Is It Pain?
Crustaceans and fish are not automatons. In the life of any organism, it's beneficial to identify harmful stimulus and move away from it.
But in the parlance of the researchers who are trying to gauge the diversity and origins of pain, there's an important difference between detecting a stimulus to be avoided, called nociception, and what we know as pain.
Nociception is the ability to pick up on a harmful stimulus and react by reflex. So far as researchers can tell, it is a knee-jerk reaction to a certain condition without an accompanying sensation. Pain, for its part, goes a step further by creating a hurtful sensation.
The most widely used definition of pain comes from the International Association for the Study of Pain, which defines the phenomenon as, "An unpleasant sensory and emotional experience associated with actual or potential tissue damage, or described in terms of such damage."
Yet this generalized definition is still limited by our experience. "A critical problem here is how we think about pain in animals," says Penn State University biologist Victoria Braithwaite.
"It's hard enough understanding a subjective, internal experience in another human being," she says, "but at least we have language to communicate and share our experiences with one another." We don't have that opportunity with other animals.
In fact, our distance from some animals makes detecting pain all the more difficult. "I'm sure our ability to empathize with other mammals has a lot to do with which animals we think will suffer from pain," Braithwaite says. "Many people find it hard to empathize with fish, and a crab or a lobster [seems] even further removed."
The key, she says, is to "take empathy out of the equation and just look at behavioral and cognitive changes" to tell how other organisms react to painful stimuli.
The latest attempt to do so was published this month by University of Belfast biologists Barry Magee and Robert Elwood. The title of their paper—"Shock avoidance by discrimination learning in the shore crab (Carcinus maenas) is consistent with a key criterion for pain"—shows how carefully researchers have been wording their conclusions.
To approach the question of crab pain, Magee and Elwood collected European shore crabs from England's Barr Hall Bay. Ninety of these subjects were fitted with a lasso of insulated copper wire around both of their fifth walking legs, the end of which was connected to an electric stimulator.
The crabs were then offered a choice of two dark shelters, but with a catch: Before the first trial, the researchers randomly determined which crabs would receive a shock upon entering the shelter, and the scientists shocked the crab whenever the individual arthropod entered the same cave in further trials. Magee and Elwood ran the tests ten times for each crab, with a two-minute break in between tests.
Some of the crabs tried to rid themselves of the wires. Ten of the crabs cast off a leg that had been fitted with the wire, only to have the loop wound around another leg. Seven of the subjects cast off the second hindered leg, and were excluded from the experiment.
The rest scuttled into the shelters without self-amputation, and crabs that received shocks during the first and second trials tended to subsequently choose the non-shock shelter. A few crabs persisted in trying to hide in the shock shelter, though, and apparently didn't discriminate like their test-mates did.
Were crabs casting off legs and avoiding the shock shelter because they felt pain? That's hard to say.
Magee and Elwood reported that many of the crabs tended to avoid the shelters they had been shocked in, and that this kind of learning "is a key criterion/expectation for pain experience." The results, the researchers noted, were consistent with a crustacean having the ability to feel pain.
Other researchers aren't so sure. University of Texas-Pan American neuroethologist Zen Faulkes pointed to two problems that might mar interpretations of the study.
For one thing, crabs don't typically encounter electric shocks during the course of their daily lives. The behavior of the crabs might be altered by the fact that the stimulus is unfamiliar to them, not by a sensation like pain.
Furthermore, the tests were run in rapid succession. Some of the crabs didn't learn their electrified lesson, and it's unknown whether those that avoided the shock shelters retained that behavior in the long term. The test showed that some crabs could learn to avoid a stimulus over the short term, but it doesn't tell us how the crabs react to the kind of tissue damage they'd normally encounter.
Even if the shore crabs truly did feel pain, this doesn't necessarily mean that all crustaceans do, or that they do in the same way.
"The distribution of pain across species is still very controversial," Faulkes says. Case studies of creatures from fish and crustaceans to leeches, fruit flies, and worms suggest that the sensory organs required for nociception are widespread, but we're still gathering case studies of how organisms react to possibly painful stimuli.
We should take care not to overgeneralize and say all crustaceans feel pain because a handful of species from different lineages do, Faulkes says.
And as Elwood points out, "Some think pain evolved within the vertebrates but at what point is not agreed." At this point, researchers can't even be sure whether pain evolved once in an ancient common ancestor or evolved multiple times in the history of life.
The case for fish pain isn't any simpler.
Penn State's Braithwaite summarized the case for piscine agony in her 2010 book Do Fish Feel Pain? She went beyond the continuing arguments over telling the difference between nociception and true pain to suggest that fish are conscious animals, and therefore they feel pain.
"Fish have a fairly stripped down, basic vertebrate brain, as such the pain they experience will necessarily be less complex than the pain we recognize and describe in ourselves," Braithwaite says, but that they still experience some sort of pain.
Carleton University's Cook disagrees.
In their paper, Cooke and co-authors assert that various experiments claiming to provide evidence of fish pain are flawed. Not only that, the researchers argue, but the mechanics of fish pain are different from our own.
We feel pain thanks to sensory neurons called nociceptors. In addition to others, we have what are called C-fiber nociceptors that allow us to feel intense, excruciating pain. Bony fish, on the other hand, don't have as many C-fiber nociceptors and instead have an abundance of A-delta nociceptors.
These neurons "serve rapid, less noxious injury signaling," Cooke and co-authors point out, that inspire the fish to avoid a stimulus without actually causing pain as we know it. The most that fish may regularly feel is the equivalent of a quick needle prick.
"Fish and inverts like those used in the recent study certainly have the ability to learn and can also respond to noxious stimuli," Cooke says, but that does not demonstrate that the organisms actually feel pain.
The same is true for Elwood's crabs. "We do not know the 'feeling' experienced by crustaceans or any other animal," Elwood says. "We can make inferences from their behavior that it is unpleasant but we cannot state that one hundred percent."
Indeed, what other organisms feel relies on definitions and designs, and our often limited ability to peer into biology. Getting a hold of seafood pain is still a slippery task.