18 January 2013

What we know and don’t know about crustacean pain

Summary

What we know about crustacean pain?

  • Crabs, and probably other big decapod crustaceans, avoid electric shock in the short term.
  • They can learn to avoid places where they were shocked over slightly longer terms.
  • There may be substantial variation across individuals in their ability to learn.
  • The evidence is consistent with pain.
  • Pain is hard to prove, even in humans.

What don’t we know?

  • Whether electric shock is normally relevant to crustaceans.
  • Whether electric shock processed in the same sort of way that people and mammals process noxious stimuli.
  • Whether there are specialized neurons for noxious stimuli in crustacean.
  • Whether any other kinds of stimuli are aversive to large crustaceans, like high temperatures.

Paper unpacking

A new paper on crustacean pain by Magee and Elwood came out on Wednesday, 16 January 2013. This new paper is, in some ways, a variation on papers that senior author Robert Elwood published on hermit crabs (Appel and Elwood 2009, Elwood and Appel, 2009). In these earlier hermit crab work, they shocked the abdomen of the crabs, and they found they could get the hermits to leave the shell and take what would normally be an inferior shell as a new home.

In the new article, Magee and Elwood used electric shock as their stimulus again. Electric shock is used in many studies of pain, but it does have a problem: it’s not very specific. It will trip off any kind of cell that is electrically excitable, including sensory neurons, motor neurons (potentially causing spikes from motor neurons to travel backwards into the central nervous system), and muscles. It’s difficult to know just what you’re doing to the animal’s nervous system.

Crabs (in this case, Carcinus maenas; pictured) like dark hidey-holes. Magee and Elwood took the crabs, placed them in an open arena with two shelters, one with vertical stripes and one with horizontal stripes. Then, they chose one shelter that if the crab entered it, they gave it an electric shock. They gave the animals 10 trials, which were delivered in short order (two minutes between each trial). The total testing time for each animal seemed to be maybe an hour or two, depending on the crab’s behaviour.

What you would expect is that crabs would learn to avoid the avoid the shelter in which they got shocked. This is indeed what happens (Figure 1 from Magee and Elwood below). But notice that even at the end of the trails, about a third of the crabs are still walking into the shock box. Maybe these these just crab masochists.


The authors went on to test whether it was the stripes on the shelter, or the direction of the shelter, that the crabs had learned by swapping the positions of the two shelters. This seemed to have happened right after the ten trials. Given that part of the argument that they make in the Introduction that “pain facilitates long-term protection because of the ease with which animals learn to avoid that situation and avoid future damage,” and in the Discussion that they are finding “long-term motivational change,” the relatively short time scale is slightly surprising. Magee and Elwood’s argument would be greatly strengthened if they showed the crabs retained the memory after, say, 24 hours or 48 hours. Other studies have shown that decapod crustaceans, like crayfish and lobsters, can remember things, such as who they’ve fought, for days to weeks (reviewed in Hemsworth et al. 2007; see their Table 1).

It’s worth comparing this to an earlier paper that had a similar approach. Kawai et al. (2004) also applied electric shock to crayfish. Those authors had two groups:

  • Crayfish shocked while facing a door they could escape through (group F for forward);
  • Crayfish shocked while they were facing away from the door (group B for backward). 

These authors noted that group F, on the right in the figure below, learned to avoid the shock. But notice that about half the animals in this group never learned the task (S6, 7, and 10), and it took a long time. Group B never improved.


Magee and Elwood mention the long training in the paper by Kawai and colleagues, but not the variation in performance either between the two groups, or within the one group. I wonder if an animal by animal breakdown in the Magee and Elwood paper would show the same sort of individual variation. That is, the Magee and Elwood figure could either be:

  1. All the crabs getting a little better throughout the trials.
  2. Some crabs getting very good, while others just never, ever learn.

Now, the crayfish were shocked less than the crabs were. But if the idea being put forward is that avoidance learning suggests pain, would this mean that only about half of crayfish feel pain... and only if they are looking at a door?

Press coverage

Having talked about the paper itself, I want to shift to how it’s being reported. I expected media attention over this paper, because previous papers from the Elwood lab had gotten attention. For instance, a lead interview on Quirks and Quarks. I was still surprised by the breadth of coverage people in my Twitter feed helped me find yesterday. The Daily Mail was the first I found, followed by the BBC, Discovery, The Guardian, National Public Radio, Fox News, Live Science and I’m sure there will be many others.

The Mail article starts off with the old hack, “Scientists have proven...” as though this is a worldwide consensus instead of two people (Magee and Elwood, 2013). Oh, but how such reports grate on me with their use of the word “prove.” (There are exceptions; the BBC puts “further evidence” in its headline, which emphasizes that this is part of a series of studies).

The original paper in JEB is, as often the case, much more nuanced than the press articles suggest. It carefully uses phrases like, “consistent with pain”, which admits there are alternative hypotheses. Elwood and colleagues are doing a series of studies, step by step; the sort of incremental progress that characterizes so much of science.

Let me start by saying that not everyone agrees with the notion generally that crustaceans feel pain. Victoria Braithwaite, in her book Do Fish Feel Pain? (reviewed here), concluded that crustaceans do not feel pain, even after long discussions with Elwood.

The two have very different standards on what they think the criteria for pain should be. Elwood appears to think that to show that an animal feels pain, you only need to show that it responds to a nasty stimulus with something more complicated than a reflex. Braithwaite thinks that to show an animal feels pain, you need to show that animal is capable of consciousness. I think it’s fair to say that neither one is widely accepted as the standard for showing an animal feels pain.

To take a similar case, the evidence for nociception in fish has been clear for a decade now: fish have neurons specialized for tissue damage. Braithwaite gave a book-length argument in Do Feel Feel Pain? why she was convinced fish feel pain. And yet, just weeks ago, a new review article by Rose and colleagues (in press) answered the rhetorical question in its title “Do fish really feel pain?” (my emphasis; I can’t see the title as anything other than a very deliberate snub of Braithwaite’s book) with a definite, “No.”

If people are still engaged in heated debates about pain in fish after ten years, even when the evidence related to the question is much further developed than it is for crustaceans, we are a long way from “proving” crustaceans feel pain.

Following along those lines of whether crustaceans need specific conditions to experience pain, I want to return to the issue of specific stimuli. Here is one of my issues with how this story is being reported:

Electric shock is not boiling water.

Many sources are immediately linking the two things under the common notion of “pain.” But only one was tested in the paper. The Daily Mail wrote:

Chefs may have to think twice before plunging live lobsters into a simmering pot. ...

The finding could have important implications for the food industry, where many chefs boil crabs, lobsters and prawns alive in the belief that they are impervious to pain.

So did Discovery:

If you’ve ever tried to boil a live lobster, you probably noticed that it did not just sit patiently in the pot. Most lobsters put up quite a struggle.

The Guardian also tied this research to cooking:

When it comes to cooking that crab for your dinner, however, it may be best to give it the benefit of the doubt.

So did Cosmos magazine (mirrored at ABC):

A lobster thrown live into boiling water may suffer for many seconds, said a scientist who argues that crustaceans can likely feel pain.

So did Fox News, and added housing into the mix.

Researchers have suspected for some time that live lobsters dunked into boiling water and rubber-banded crustaceans stored in crowded fish market tanks experience tremendous pain.

Even if you agree that electric shock is painful to the crabs, that does not automatically mean that crabs experience pain the same way we do. It’s not a crazy hypothesis, but it is still something to be tested rather than something that has already been demonstrated. For instance, at the recent Society for Integrative and Comparative Biology meeting, one talk showed a short clip rather like this one.


It shows a crab, its claw injured in a fight, crabbing its claw, and ripping it off. You could hear the audience reacting when this was shown; people made the sort of groans that they make when they see the weekly sports blooper reel, particularly when you see accidental hits in the groin area.

Here’s a shorter, (but off-colour!) video of the same behaviour.


This is a reminder that what might seem painful to us is not necessarily painful to a different animal. Tearing off a limb voluntarily is not something a human would do.

Let me give you another quick example.

In humans, capsaicin is the chemical that makes chili peppers hot, and is often used in studies of pain as a painful stimuli. Strictly speaking, the chemical causes sensory neurons called nociceptors to fire. Fruit flies also have nociceptors , so at first blush, it’s perfectly reasonably to think they would avoid food laced with capsaicin.

Nope. The more capsaicin, the more the flies like the food (Al-Anzi et al. 2006). Live Science also earns points in my book for mentioning that naked mole rats do not respond to many stimuli that other mammals avoid and appear painful.

If you want to know if boiling a lobster is painful to said lobster, you should test its response to high temperatures, not electric shock.

It is heartening to see that some of the articles I’ve found obviously used embargo time to find other scientists to comment on the study. Scientists who study fish (Paul Hart, quoted in The Guardian; Lynne Sneddon, quoted by the BBC; Lynne worked on fish nociception, so was a good choice), marine organisms besides decapod crustaceans (Magnus Johnson, also quoted in The Guardian). Only one reported contacted someone who has worked on crustacean behaviour (Francesca Gherhardi, who I just met last week, quoted by Live Science).

Having provided several papers providing evidence that electric shock is painful, I am surprised that NPR reports that Elwood suggests electrocuting crustaceans is a pain-free way of dispatching them.

As for what this might mean for those of us who occasionally dispatch a crustacean or two, the best way to minimize potential pain is likely electrocution or driving a knife through the creature's brain, Elwood says. But as most of us lack specialized machinery and knowledge of crustacean anatomy, the easiest way is still dropping the crab in a pot of boiling water.

I’ve commented on this before (here, here). In crustacean neurobiology labs, the most commonly used anaesthetic for crabs, crayfish, and lobster, is chilling. My suggestion would be to put an animal on crushed ice.

I do not have strong opinions about whether crustaceans feel pain or not. But I do think that this new paper is closer to the beginning of research on this kind of question than it is to the end.

Additional: I find it interesting that The Independent ran this story in their “Food and drink” section.

References

Al-Anzi B, Tracey Jr. WD, Benzer S. 2006. Response of Drosophila to wasabi is mediated by painless, the fly homolog of mammalian TRPA1/ANKTM1. Current Biology 16(10): 1034-1040. http://dx.doi.org/10.1016/j.cub.2006.04.002

Appel M, Elwood RW. 2009. Motivational trade-offs and potential pain experience in hermit crabs. Applied Animal Behaviour Science 119: 120-124. http://dx.doi.org/10.1016/j.applanim.2009.03.013

Braithwaite VA. 2010. Do Fish Feel Pain? Oxford: Oxford University Press.

Elwood RW, Appel M. 2009. Pain experience in hermit crabs? Animal Behaviour 77: 1243-1246. http://dx.doi.org/10.1016/j.anbehav.2009.01.028

Hemsworth R, Villareal W, Patullo BW, Macmillan DL. 2007. Crustacean social behavioral changes in response to isolation. The Biological Bulletin 213(2): 187-195. http://www.biolbull.org/cgi/content/abstract/213/2/187

Kawai N, Kono R, Sugimoto S. 2004. Avoidance learning in the crayfish (Procambarus clarkii) depends on the predatory imminence of the unconditioned stimulus: a behavior systems approach to learning in invertebrates. Behavioural Brain Research 150(1-2): 229-237. http://dx.doi.org/10.1016/S0166-4328(03)00261-4

Magee B, Elwood RW. 2013. Shock avoidance by discrimination learning in the shore crab (Carcinus maenas) is consistent with a key criterion for pain. The Journal of Experimental Biology 216(3): 353-358. http://dx.doi.org/10.1242/jeb.072041

Rose JD, Arlinghaus R, Cooke SJ, Diggles BK, Sawynok W, Stevens ED, Wynne CDL. 2012. Can fish really feel pain? Fish and Fisheries: in press. http://dx.doi.org/10.1111/faf.12010

Related posts

Ignorance may not be bliss, but perhaps it is painless

Crustacean nociception: Origins, part 1

Crustacean nociception: Origins, part 2

Crustacean nociception: the worry

Shell shock

Shell shock, revisited

Tenth International Congress for Neuroethology, Day 5 (nociception symposium coverage)

External links

The Daily Mail: Lobsters and crabs can feel pain and take action to avoid it happening again

Live Science: Crabs really do feel pain: Study (Mirrored by Huffington Post: Crabs Feel Pain After All, New Study Suggests)

NPR The Salt: Yes, Virginia, Crabs Likely Feel Pain, But They're Still Delicious

Fox News: Lobsters, crabs feel pain, scientists say

BBC: Further evidence crabs and other crustaceans feel pain

The Guardian: Crab study puts pain on the menu

Cosmos magazine: Be kind to your seafood, study urges

Australian Broadcasting Corporation (ABC) Science: Be kind to your seafood, study urges

The Independent: Shock survey: Lobsters and crabs feel pain

Crab photo by BrentMWilson on Flickr; used under a Creative Commons license.

4 comments:

Ryan.O said...

Hi there,

A good piece and an interesting review of the paper and its subsequent write up in the news. It's a fascinating field of research that deserves more than the limited word count we're often limited too.

I would just like to say that it was Professor Paul Hart, and not Hunt, this was an error and has since been amended on the Guardian site. Please update accordingly.

Also, on a final note, Prof Elwood, Dr Johnson and Prof Hart all gave great insight and provided a balanced view of the study and the use of the term 'pain'. It's a complex field of research which polarises opinion.

All the best,
Ryan

biobabbler said...

The question I always ask is "Why wouldn't a (insert animal species/group name) feel pain?"

Clearly it's adaptive to try and reduce damage to your body, avoid bleeding (which attracts predators and may end your life), etc. And pain is a very quick, effective (and thus, exceedingly common) way to perceive that X situation is damaging your body. (Of course I'm not addressing about pain that some animals might endure in order to mate or raise their offspring, as that may be adaptive...)

I have little faith in our ability to accurately perceive other animals' experiences, so am not a big fan of "clip X species feet off and see if they still walk, and if they do, that proves they do not feel pain" experiments. (not making that experiment up)

I'm not sure it's a great use of time or $ or animals. Or entirely ethical.

I'd just assume most animals experience pain, because it makes a LOT of sense re: evolutionary theory, and move on to the next topic. Like how to conserve the species that exist right now, regardless of whether or not we believe they feel pain.

Zen Faulkes said...

Ryan: Thanks for that correction; I’ve fixed my text.

Biobabbler: There's a very subtle, and tricky, distinction here. There is a difference between “pain” and “nociception.” Pain is usually defined as having a psychological element. Nociception is sensory detection of tissue damage. To give one quick example of how they differ, phantom limb pain is pain without tissue damage; there is literally no tissue to damage.

You made the adaptive argument for pain, but “pain” could be easily replaced with “nociception,” and you would have the same argument. The problems are:

1. Where does nociception alone stop and pain begin? People do not agree on this. Elwood sees nociception as something that can only trigger a pure reflex. I see nociception as sensory information that can be used in many ways.

2. What does pain bring to an adaptive argument that nociception alone does not?

It’s much easier to get a handle on whether an animal has nociception than whether it has pain.

Alpha said...

I was trying to figure out what to do with shrimp after I catch them so I won't cause them too much pain when they are beheaded , de-veined , cooked , etc. .

Zen Faulkes has suggested using crushed ice to cool the shrimp to dull their senses .

Adding salt or brine is one way to make the crushed ice colder . I have read that subzero temperatures can be made by making a slurry of crushed ice and cold , concentrated salt water .

Perhaps the shrimp could be salted , and iced with a bit of cold sea water added/retained ?