A new paper by Kasiouras and colleagues attempts to provide evidence for nociceptive neurons in a decapod crustacean, a shore crab.
The authors took crabs, poked them and dropped some acid on them, and recorded the neural responses. Neurons did indeed respond, in dose-and intensity specific ways. From this, the authors conclude these are potential nociceptive responses.
I am unconvinced. There is a big difference between showing that neurons can respond to a
possibly noxious stimulus and showing that those neurons are responding as nociceptors.
First:
The same category of stimuli can have detected by by nociceptors and by “regular” sensory neurons that are not nociceptors. For example, an increase in temperature can stimulate both nociceptors and thermoreceptive sensory neurons. Mechanical pressure can stimulate both mechanoreceptors and nociceptors. That there are two neural pathways are probably why we distinguish a burn (painful) as different than heat, or a pinch from a strong touch.
The results would be more convincing if the authors showed that neurons responded in ways that are typical of other nociceptors. Many (though not all) nociceptors have a few common properties.
They respond to several different types of stimuli. For example, they react to high temperature and acid and mechanical pressure and a chemical like capsaicin. (The technical term is that they are polymodal or multimodal sensory neurons.)
They respond to repeated stimulation with increased activity. Most sensory neurons “get used to” the same sensory stimuli over time, but many nociceptors do the opposite. (The technical term is that they show sensitization.)
The authors couldn’t do either of these, because they are recording from the whole
nerve cord and they did not pick out the activity of single neurons. Sometimes it is possible to recognize the activity of single neurons in this sort of record with spike sorting techniques, but that is done in this paper.
Second:
Species respond to potentially noxious stimuli in different ways. Some species respond to capsaicin with nociceptive behaviours, but others do not. No stimulus is guaranteed trigger nociceptors in all cases.
This paper used mechanical touch and acetic acid, but because the paper did no behavioural experiments, it’s not clear if the crabs perform nociceptive behaviour in response to the level of stimuli presented.
Another paper used acetic acid as a potentially noxious stimulus with
shore crabs, and crabs do respond to it (Elwood et al. 2017), but that
paper was criticized (Diggles 2018; not cited in the current study) for not considering the possibility that acetic
acid caused a feeding (gustatory) response, not a nociceptive response. Acetic acid is the
technical name for vinegar, after all.
The results would be more convincing if the electophysiological recordings of neurons were connected back to the crab’s behaviour. For example, the authors could tried an experiment to shown that a touch of low intensity caused one sort of behaviour, but a touch of higher intensity caused a different behaviour that looks like nociceptive behaviour. Then they could have seen what the differences in neural activity to those two kinds of tactile stimulation were.
I am glad to see more labs trying to establish the presence or absence of nociceptors in crustaceans. There is still more work to demonstrate their existence and characterize their physiology if they exist.
References
Diggles BK. 2018. Review of some scientific issues related to crustacean welfare. ICES Journal of Marine Science: fsy058. http://dx.doi.org/10.1093/icesjms/fsy058
Elwood RW, Dalton N, Riddell G. 2017. Aversive responses by shore crabs to acetic acid but not to capsaicin. Behavioural Processes140: 1-5. https://doi.org/10.1016/j.beproc.2017.03.022
Kasiouras E, Hubbard PC, Gräns A, Sneddon LU. 2024. Putative nociceptive responses in a decapod crustacean: The shore crab (Carcinus maenas). Biology13(11): 851. https://doi.org/10.3390/biology13110851
Picture by Dunnock_D on Flickr; used under a Creative Commons license.
From time to time, I see people say that some group of animals have nociceptirs or "pain receptors" amd then use to to say this prooves those animals feel pain.
There is a lot of subtle misuse of definitions going on there.
Nociceptors are neurons tuned to tissue damage. Pain is not tissue damage. The two are related but they are not the same.
Calling nociceptors “pain receptors” is like calling auditory sensory neurons “music receptors.” And then use that animals can hear to claim that animals appreciate music. Well, no. There is a difference between sensory neurons and a higher order perception or psychological state arising from those sensory signals.
I was saddened to learn about the untimely death of Victoria Brathwaite. Victoria was a pioneer in research on nociception in non-mammals (fish, specifically), culminating in her book Do Fish Feel Pain? (reviewed here).
I was fortunate to have her as one of the speakers for a symposium I co-organized for Neuroethology in 2012. She was a fine speaker, and I’m sorry I won’t get more chances to interact or learn from her.
This morning I learned of the UK advocacy group “Crustacean Compassion”, which wants to change laws around the handling of crustaceans in the United Kingdom. They are currently engaged in a campaign to recognize the decapod crustaceans as having “sentience.”
They claim to be an “an evidence-based campaign group,” but when I went to their tab on whether crustaceans feel pain, I was presented with a one-sided view. Not lopsided. One-sided.
All the evidence comes from one lab, that of Professor Robert Elwood.
Weirdly, the page is so singularly built from Elwood’s work that it even omits research from other labs that could be viewed as supporting their premise that decapod crustaceans might feel pain.
They present experiments that have not been independently replicated as though they were unquestioned. They discuss none of the interpretive problems behind those experiments. They act as though there is a clear consensus within the scientific community when there is not (review in Diggles 2018).
Their full briefing for politicians is similarly one-sided.
In science, single studies are not definitive. Studies all arising from a single lab are not definitive.
If you claim to be all about the evidence, you have to present all the evidence, not just the evidence that supports your position. Some of the individuals behind the group have academic and scientific backgrounds, but judging from their bios, none have training working with invertebrates. None have training in neurobiology.
While I have reservations about the information provided by their group, the part of me that loves graphic design gives them full points for their clever logo (shown above).
References Diggles BK. 2018. Review of some scientific issues related to crustacean welfare. ICES Journal of Marine Science: fsy058. https://doi.org/10.1093/icesjms/fsy058
Puri S, Faulkes Z. 2015. Can crayfish take the heat? Procambarus clarkii show nociceptive behaviour to high temperature stimuli, but not low temperature or chemical stimuli. Biology Open4(4): 441-448. https://doi.org/10.1242/bio.20149654
I’ve been studying issues roiling around the question of “Does it hurt lobsters when they go into a pot?” for about a decade. After ten years or so, you get a little jaded. I’m used to seeing the same bad arguments. I’m used to it popping up and making the rounds in news about twice a year. The first time this year was when Switzerland put laws into place about lobster handling. This is the second.
And I’ve got to say:
That’s new.
A Maine newspaper is reporting on a restaurant owner, Charlotte Gill, is sedating lobster with marijuana.
I am pretty sure cannabis as a sedative not been the subject of any peer-reviewed scientific papers on crustacean anesthesia. But a quick Google Scholar search (thank you thank you thank you Google for this tool) shows that spiny lobsters and other invertebrates have cannabinoid receptors (McPartland et al. 2005). This makes the technique plausible on the face of it.
The behavioural effects reported were interesting.
Following the experiment, Roscoe’s (the experimental lobster - ZF) claw bands were removed and kept off for nearly three weeks.
His mood seemed to have an impact on the other lobsters in the tank. He never again wielded his claws as weapons.
I am surprised by the apparent duration of the effects. Weeks of behaviour change from a single treatment? That seems long compared to soporific effects of marijuana smoke in humans doesn’t seem to last multiple days.
Earlier this week, Roscoe was returned to the ocean as a thank you for being the experimental crustacean.
I’m not sure of the ethics of this. Will Roscoe the lobster, who has apparently forgotten how to use claws, going to become a quick meal for a predator? A lobster without claws in the ocean is just bait (Barshaw et al. 2003). Releasing Roscoe may doom him!
I am a little concerned by what seems to be Gill’s quick dismissal of other techniques:
In Switzerland, the recommended method of cooking the crustacean is to electrocute it or stab it in the head before putting it in the boiling water.
“These are both horrible options,” said Gill. “If we’re going to take a life we have a responsibility to do it as humanely as possible.”
I don’t know if she has anything but intuition to support that opinion. There’s research on electrical stunning, and the results so far are mixed. Fregin and Bickmeyer (2016) found shocks “do not mitigate the response to external stimuli,” but Neil (2012), Roth and Grimsbø (2016), and Weineck et al. (2018) found electric shocks seemed to knock down neural activity effectively. But the impression I get is that using shock is tricky: you need different protocols for different animals.
It’s also worth noting that a new paper by Weineck et al. (2018) showed chilling was effective as an anesthetic, which the Swiss regulations forbade. Research I co-authored (Puri and Faulkes 2015) showed no evidence that crayfish responded to low temperature stimuli.
Of course, another complication around this technique is its legality. The legal landscape around marijuana in the U.S. is tricky. Marijuana is still regulated federally, but certain states permit different kinds of uses. The article notes:
Gill holds a medical marijuana caregiver license with the state and is using product she grows in order to guarantee its quality.
This is interesting, but it’s not clear to me that this is a more cost effective or humane way to sedate a lobster than what many crustacean researchers have been doing for a long time: cooling on crushed ice.
Barshaw DE, Lavalli KL, Spanier E. 2003. Offense versus defense: responses of three morphological types of lobsters to predation. Marine Ecology Progress Series256: 171-182. https://doi.org/10.3354/meps256171
Fregin T, Bickmeyer U. 2016. Electrophysiological investigation of different methods of anesthesia in lobster and crayfish. PLOS ONE11(9): e0162894. https://doi.org/10.1371/journal.pone.0162894
McPartland JM, Agraval J, Gleeson D, Heasman K, Glass M. 2006. Cannabinoid receptors in invertebrates. Journal of Evolutionary Biology19(2): 366-373. https://doi.org/10.1111/j.1420-9101.2005.01028.x
Puri S, Faulkes Z. 2015. Can crayfish take the heat? Procambarus clarkii show nociceptive behaviour to high temperature stimuli, but not low temperature or chemical stimuli. Biology Open4(4): 441-448. https://doi.org/10.1242/bio.20149654
Roth B, Grimsbø E. 2016. Electrical stunning of edible crabs (Cancer pagurus): from single experiments to commercial practice. Animal Welfare25(4): 489-497. https://doi.org/10.7120/09627286.25.4.489
Weineck K, Ray A, Fleckenstein L, Medley M, Dzubuk N, Piana E, Cooper R. 2018. Physiological changes as a measure of crustacean welfare under different standardized stunning techniques: cooling and electroshock. Animals8(9): 158. http://www.mdpi.com/2076-2615/8/9/158
A side effect of my bafflement yesterday over how lobsters became some sort of strange right-wing analogy for the rightness of there being winners and losers (or something) was getting into a discussion about whether lobsters have brains.
That decapod crustaceans are brainless is a claim I have seen repeated
many times, often in the service of the claim that lobsters cannot feel
pain. This article, refuting Jordan Peterson, said:
(L)obsters don’t even have a brain, just an aglomerate of nerve endings called ganglia.
This is a bad description of ganglia. It makes it sound like there are no cell bodies in ganglia, where there usually are. Here are some. This is from the abdominal ganglion of Louisiana red swamp crayfish (Procambarus clarkii):
These show cell bodies of leg motor neurons from several species (sand crabs and crayfish, I think; these pics go back to my doctoral work).
These are neurons in a ganglion from a slipper lobster (Ibacus peronii), where those big black cell bodies are very easy to see:
And these are leg motor neurons in slipper lobster:
And we’re know this for well over a century, as this drawing from 1890 by master neuroanatomist Gustav Retzius shows:
So ganglia are more than “nerve endings.” So putting that aside, are there other features that make brains, brains?
Intuitively, when I think about brains, I think of a few main features. Two anatomical, and one functional:
Brains are big, single cluster of neurons. Even though there may be many neurons in, say, the digestive system (and there are not as many as some people claim), it’s so diffuse that nobody would call it a brain.
It’s in the head, near lots of sensory organs. In humans, our brain is right next door to our eyes, ears, nose, and mouth, which covers a lot of the old-fashioned senses.
It’s a major coordinating center for behaviour.
Decapod crustaceans (not to mention many other invertebrates) meet all those criteria. Sure, the proportion of neurons in the decapod crustacean brain may be smaller than vertebrates, but I have never seen a generally agreed upon amount of neural tissue that something must have to be a brain instead of a “ganglion in the front of the animal.”
I have a sneaking suspicion that some people will argue that only vertebrates can have brains because we are vertebrates, and vertebrates must be special, because we are vertebrates. That is, people will define brains in a way to stroke human egos.
And, as I implied above, some people make the “no brains” claim out of self-interest. I don’t think it’s any accident that I see “lobsters don’t have brains” coming from institutes that have close ties to commercial lobster fisheries.
I suppose that some could argue that limiting the word “brain” to vertebrates is a way of bringing recognizing that vertebrate and invertebrate nervous systems are structured very differently. They are, but why only do this for one part of the nervous system? This
is a little bit like saying “invertebrates don’t have eyes,” because they
have compound eyes instead of our camera-style eyes. We routinely give things in invertebrates and vertebrates the same names if they have the same functions.
And in practice, I see people referring to octopus brains all the time. They do so even though, like other invertebrates, a large proportion of the nervous system sits outside the brain. From memory, roughly half the neurons in an octopus reside in its arms.
In practice, I am far from the only person that calls the clump of neurons at the front end of decapod crustaceans, “brains.” From this page:
So, fellow neuroscientists, if you don’t think invertebrates can have brains, why not? What is your dividing line?
At the start of this week, I saw a news story about new Swiss regulations for the handling and killing of lobsters. (Coincidentally, it came very shortly after this very good article about similar issues around fishes.) This started with a motion by Green Party politician Maya Graf. She wanted to ban lobster imports into Switzerland outright, but Switzerland already had a trade agreement with the European Union that ruled that out.
This is the short version of the Swiss law (auto-translated from German):
The lobster is better protected in the future
Lobster and other crayfish may no longer be transported on ice or in ice water. This is important for the import to Switzerland. All species living in water must always be kept in their natural environment - this also applies to the lobster. In addition, crayfish must be stunned before being killed. The usual dipping in the gastronomy not stunned lobster in boiling water is therefore no longer permitted.
Further information: Articles 23 (1), 178 and 178a of the Animal Welfare Ordinance .
New scientific evidence shows that crayfish are just like vertebrates, sentient and capable of suffering.
But it does not summarize what scientific evidence was examined and used to justify this decision. However, the Swiss website links to a document from the Australian Royal Society for the Prevention of Cruelty to Animals (RSPCA), which implies they agency agrees with the material contained within. The RSPCA document does have a reference list of research papers, with the most recent references dating to 2015.
The RSPCA document is not intended to be a scientific literature review. But that it does cite scientific papers can give an impression of greater certainty and consensus in the scientific community than is perhaps warranted.
For context, and in the interests of full disclosure, there are very few research groups have published empirical behavioural data about crustacean noceiception. One is led by Roger Elwood, and another is led by me. There are a few other papers from other places.
First, two research labs is a small fraction of the crustacean research community. Even if those two labs were entirely in agreement about the data (the two labs have contradictory results on one effect) and the interpretation of those data, two labs should not be taken to represent a broad scientific consensus. A 2014 book on crustacean nervous systems and behaviour alone has somewhere around 30 authors, none of which are from the two labs I mentioned.
Second, the RSPCA document cites only Elwood’s papers. (In fairness, the most relevant paper I co-authored on this subject was in 2015, the same year as the newest paper in the RSPCA document. That paper may have been too new to make it into the RSPCA document.)
Third, not all researchers examining the data are in agreement, even those with expertise in the relevant issues. In her book Can Fish Feel Pain? (reviewed here), Victoria Brathwaite describes having long conversations with Elwood about this topic. Despite Elwood’s arguments, Braithwaite concluded that lobsters do not feel pain. Joe Ayers (who was an examiner on my Ph.D.) also disagrees.
Fourth, the papers cited by the RSPCA do not claim that lobsters (and other large decapod crustaceans) are sentient, nor do they claim that they suffer. The papers are appropriately cautiously worded, and say the results are consistent with crustacean pain. Elwood has said this when speaking to scientists. “Consistent with” means “not ruled out.” It doesn’t necessarily mean likely. But when speaking to the general press, Elwood has said lobsters probably feel pain. As quoted above, the Swiss Q and A goes even further and says lobster pain has been shown.
And thus do we move from “possible” in data, to “probable” in the public eye, to “definite” in law.
The specifics of the policies are also puzzling. It forbids lobsters from being transported on ice. It is not clear in my translation (“Direct contact with ice or iced water can cause cold in the animals damage arises.”) if this is because of concerns about “pain”. A paper I co-authored in 2015 that showed crayfish do not avoid very low temperature stimuli.
The law seems to require that lobsters and crayfish are anaesthetised before being killed (Google translates the word as “stunned,” but this doesn’t seem to refer to electrical stunning). But when you ask crustacean biologists how to aneasthetize crustaceans, one common answer is, “Put them on ice.” Even the Q and A recommends cooling lobsters before killing them. It’s not clear why cooling is recommended but ice is illegal.
(T)here’s no scientific evidence to support the position.
The material quoted as being from the Lobster Institute is, like the Swiss law, far more confident than the data suggests. The article pulls out the “lobsters have no brain” myth. We have known for more than a century they do have brains. Absolutely nobody knows what the minimal amount of nervous system is for generating “pain.”
The recommendations for killing lobsters in the RSPCA document are generally consistent with what I do when using decapod crustaceans for research. (Image also shows up here.) The image at the top of this post shows how I was taught to sacrifice decapod crustaceans in a humane way. It is not the only way, but I think it is reasonable and fairly easy.
I agree with the goals of this law. You should be careful in handling and killing animals rather than careless. But it’s not a strong model for science informing policy.
P.S.—One interesting tidbit I learned in perusing the Swiss documents is that Crustastun (which I wrote about eight years ago; see also here) makes no equipment, according to the Swiss Q and A document.
I just learned that an answer I wrote months ago on Quora got picked up and featured on a fairly major UK news website, the Independent months ago.
You never know how far something you put online might travel. Or how hard it might be to know that it has traveled. I had no idea it was on the Independent website until a few minutes ago.
From the Weekly World News, 17 September 2002. You must click to enlarge to fully appreciate the photo...
I’m surprised that nobody has taken this as evidence of immortal lobsters. I do want to use the “lobster facts” call out the next time I talk about crustacean nociception:
They have no cerebral cortex – which means they feel no pain.
Just realized that the recent crustacean nociception paper I co-authored is in the top ten most read articles for the third month running in Biology Open! It was #2 for April, #6 for May, and #6 again for June.
Thank you to all who have taken an interest and read this!
Having a couple of papersaccepted in the last few days (hooray!) reminded me that I haven’t told the story behind the most recent paper I co-authored, which came out a couple of months back.
Here, for instance, is some video we shot testing one of our stimuli. The description of this in the paper ended up being written in typical academese:
One author (Z.F.) ate representative slices of the peppers, similar to those fed to the subjects, to confirm that there were noticeable differences in pungency, and the habanero slices were unpleasantly pungent.
But here’s what really happened:
Very early on in the process of working on this project, Sakshi and I were pretty confident that we were going to have two papers. We had plans to to behavioural and physiological experiments testing the responses of crayfish to acids and bases, and to chemical stimuli like capsaicin (the stuff that makes chilies hot).
Our first plan was that the first paper would be just the behaviour, and the second paper would be all the physiological recordings or neural activity.
Well, that plan didn’t survive contact with the enemy (a.k.a. reviewer #2). Journals kept rejecting our manuscripts that had only behavioural experiments. We decided that instead of dividing the experiments up by technique, into “behaviour” and “physiology” papers, we would divide them up by the stimuli, into “pH, with both behaviour and physiology” and “chemical stimuli, with both behaviour and physiology” papers. As soon as we did that, our first paper got accepted.
The experiments for capsaicin and isothiocyanate were locked down even before the first paper came out. You can see them in the poster at right, done for a conference just a few months after Puri and Faulkes (2010) came out.
What held up this new paper was experiments for high and low temperature.
We wanted to test high temperature, but it took us a while to figure out how to do it. We were concerned about the animals. We’re not in the business of torturing crayfish here. We wanted to give the animal a way of getting away from the stimulus if it wanted to.
Inspired by Dan Tracey’s paper on fly nociception (Tracey et al. 2003), we tried using a soldering iron as a noxious high temperature stimulus. Our original idea was to let the crayfish grab the tip of the soldering iron, and measure how long it was before it would let go. This turned out not to be practical, because crayfish don’t like grabbing hard things. But in our preliminary tests, it was clear that just touching the claw got a reaction from them when it was hot, much more so than when it was room temperature.
We have a plot of the behaviour in the paper, but the video is so clear:
A positive result was a first for this project. I’m always telling people that one of the advantages of working with crayfish are that “They’re cheap as dirt, and tough as nails.” Crayfish had been oblivious to everything else we’d thrown at them, and this was the first thing that bothered them. We were very curious as to whether a positive result would make this paper have an easier ride than our first paper, which kept saying, “Nope, nothing here, either.”
While we continued the work, we presented this work at the 2011 Neuroscience meeting. Sakshi wrote about here experience here. I met lots of online people for first time, including Scicurious, Doc Becca, KatieSci, Namnezia, and too many more to mention at Doc Becca’s BANTER party.)
The feedback on the poster was good, but a key moment was when I saw another poster by Brenner and Gereau (whose work was later published in PLOS ONE, in 2012). They had come up with a simple way to test for low temperature nociception: use dry ice. Brilliant!
And the moral of this part of the story is: Don’t skip the poster sessions at conferences!
After the conference, we ran the behavioural tests for low temperatures.
We’re now around the start of 2012 with this project. And this is where we kind of got stuck, which was my fault. From the experience with our first paper, we were pretty sure this wouldn’t got anywhere without the physiology. But we couldn’t get enough physiology experiments in the can.
Unfortunately, moving from stimulating the antennae (which we’d used for acids and bases and chemicals) to the claws had created a problem. It turned out that recording from the nerve in the claw is trickier than the antennae. Trying to get what we considered the bare minimum number of recordings of the neuron turned out to be hard enough that we ultimately abandoned it. The Neruroscience poster is one of a couple of posters where we presented neural activity from the claw. The claw stuff just didn’t make it into the final paper.
We also had to change the stimulus when we tried to record action potentials. We couldn’t stick a soldering iron tip in water, but the tissue needed to be a saline solution. Plus, the soldering iron introduced electrical noise, making it impossible to see action potentials. We would have liked to have used the same stimulus, but it wasn’t possible.
We decided to move back to the antennae, because we knew we could get good neural recordings from those (we’d published a lot of them in the 2010 paper). If I remember right, I starting doing the physiological recordings there first, before doing the behavioural experiments. I knew that reviewers would savage the paper if I had behavioural and physiological data from two different parts of the crayfish. Fortunately, the antennae experiments were clear – the crayfish acted differently to hot and control – although not as interesting to watch as the claw experiments.
And Sakshi completed her bachelor’s degree along the way and got a job.
So after many, many reminders from my co-author that we needed to get this out, submissions, rejections, workshopping it in journal club, resubmission, and final revisions, I was so pleased that this paper finally found a home.
To promote it on social media, I created some memes. These were fun to make. I think you’ll need to click this one to enlarge to read it:
I did one for hot, so I needed another for cold:
I’ll probably go to hell for this next meme, but I couldn’t resist:
The pre-print went up in March, and was the #2 more read article that month! This pleases me. I was hoping we’d top that, once the paper moves from “early edition” to the final volume.
Alas, “number one with a bullet” eluded us. But in May, we were still in the top ten!
I will admit that I thought we might get a little more media attention on this paper. “Does it hurt crustaceans when you boil them alive in the pot?” is such a common question, and this paper addresses that issue more directly than anything published before.
But there is little more satisfying than seeing a long project completed and published.
Puri S, Faulkes Z. 2015. Can crayfish take the heat? Procambarus clarkii show nociceptive behaviour to high temperature stimuli, but not low temperature or chemical stimuli. Biology Open4(4): 441-448. http://dx.doi.org/10.1242/bio.20149654
In our most recent paper on nociception, one of the major points is that not all animals react to potentially nasty stimuli the same way. And it turns out that there’s a very nice demonstration of that idea on Mythbusters. In the 2008 Shark Week “Jawsome Special,” the Mythbusters did a segment called “Spicy Salsa Shark Shield.”
They showed that sharks were not deterred by the presence of capsaicin-laden material.
I included this in the references as:
Dallow, A. and Lentle, T. (2008). Mythbusters: Shark Week Special 2, Episode 102. Discovery Channel, USA: Beyond Entertainment Limited.
The journal copy editors wrote:
Only peer-reviewed references are permitted in the reference list.
I took it out, because there were other references that made the point about how responses to noxious stimuli varied from species to species. It wasn’t worth fighting over, and I think I’d have lost.
Regardless of the esteem you hold for the work done by Mythbusters, the journal’s citation policing raises bigger issues. A current trend in academic publishing is to broaden the kinds of research products that people can get academic credit for. Why should only publications “count,” and not sharing a database, or writing useful code?
Consider figshare, the cloud storage data archiving service. One of their big selling points as a data repository is that they generate digital object identifiers (DOI) for stuff submitted there. The DOI itself is not the selling point, but they strongly imply that this makes whatever is archived on Figshare citable in scholarly publications. Here’s the top from their “about” page: making things citable is the first thing the list. (my emphasis):
figshare is a repository where users can make all of their research outputs available in a citable, shareable and discoverable manner.
But all those hopes can be dashed by a single sentence from a journal. “Nope, we only take peer reviewed papers.”
Interestingly, the journal let us keep in a couple of conference abstracts. The abstracts were in published in a peer-reviewed society journal, but the abstracts themselves were not peer-reviewed.
I’ve noted before that some journals have had a tradition of allowing people to cite “grey literature,” like conference abstracts, newspaper articles, web pages, or tweets. I think that is a positive thing. I worry that this sort of “journals citing (and therefore promoting) journals” policy might become more common as journals compete for scientific products. Such policies could hamper the development of academic publishing innovations.
Even worse, a “journal only” policy has the potential to force authors into intellectual dishonesty. “We got this idea from another lab’s data on figshare, but we can’t say that in the paper, so we’ll just have to say something else.”
Authors and possibly reviewers should be determining what is a legitimate citation on a case by case basis, rather than a journal setting a blanket policy favourable to itself.
I currently still have my head down, writing, writing, and doing more writing, but I took a little time to talk to Jane Lee, who was reporting on a new paper by Robyn Crook and colleagues in Current Biology about invertebrate nociception.
I said:
This study is one of the few experiments that have looked at pain in a context closer to real-world conditions, says Zen Faulkes, an animal behavior researcher at the University of Texas-Pan American in Edinburg, Texas, who was not involved in the project. Specifically, the study looked at pain in the context of a predator-prey interaction rather than as an isolated sensation in an individual.
It’s a very interesting and cool paper. This is the key figure:
The left two columns are uninjured squid. A squid with no injuries has about a 75% chance of escaping fish predators.
The right two are injured squid. An injured squid 50% chance of escaping hungry fish.
But if the squid has injury, and is given a painkiller (IA in rightmost column = injured with analgesic, or a painkiller), the squid only have about a 25% chance of escaping a predator. In other words, the nociception system is helping the squid do better in the wild than if it didn’t have that sensory information.
“Does this invertebrate animal feel pain?” As Noah Gray noted, mass media seems to cover some version of this question about every six months or so.
This time, we have an article that appeared a few weeks ago from New Scientist. It’s just been picked up in The Washington Post and a Popular Scienceblog. The piece features the work of Robert Elwood, Robyn Crook (both of who have appeared on the blog before) and Hans Smid.
It’s an extremely good article that captures a lot of the nuances of the issue. I was surprised, though, to read this paragraph describing Elwood’s work:
(Elwood) started with prawns. After so many years of working with them, he thought he knew what to expect, which was that he would see nothing more than reflex reactions. But to his surprise, when he brushed acetic acid on their antennae, they began grooming the treated antennae with complex, prolonged movements of both front legs. What’s more, the grooming diminished when local anesthetic was applied beforehand.
Elwood is describing work he co-authored back in 2007 (Barr et al., 2007). What this fails to mention is that this effect could not be replicated in other species (Puri and Faulkes 2010). Elwood knows this; he’s mentioned the failure to replicate in his academic papers (Elwood 2011, page 177):
One recent study, however, failed to detect nociceptors in decapod crustaceans and also noted little ability to respond to noxious stimuli (Puri and Faulkes 2010) despite organized responses to noxious chemical and electrical stimuli noted in other studies (Barr et al. 2007; Elwood et al. 2009; Elwood and Appel 2009).
I’m curious as to whether this was mentioned during the interview, or was removed to get the article to the appropriate word count.
How should scientists, and reporters, discuss work that has failed to replicate? The original Barr and colleagues article remains in the scientific literature; failed replication alone is not grounds for retraction. In that sense, the paper by Barr and company has not been definitively shown to be flawed or wrong. But being able to replicate effects is an acid test (no pun intended) for determining if those effects are real and robust.
Reporters often go after quotes from outside experts; “scientists who were not involved in the study.” This is good practice, and represents due diligence on the part of the reporter to find potentially critical viewpoints. But these external experts are often working from their knowledge of the field, and are generating critiques from theory and first principles. It’s not common for them to have done any experiments.
If it’s good practice to get responses from other researcher making criticisms with no data, surely it’s even better practice to talk about criticisms that are backed up with data published in peer reviewed journals?
The paragraph I quoted above also does not mention an interpretive problem. “Grooming” is the behaviour that is used to indicate nociception and/or pain in the shrimp. Acid causes an increase in grooming. Local anesthetic applied after acid reduces grooming. So far, so good.
What would you predict if you applied anesthetic alone?
The anesthetic should not be noxious – it is supposed to reduce sensory input, after all – so you might predict to see no increase in grooming compared to control.
But applying anesthetic alone causes an increase in grooming (Figure 1 in Barr et al. 2007):
I don’t know what to make of this, except that it complicates the story. The shrimp are clearly detecting the anesthetic and responding to it in the same way as the noxious stimuli: increased grooming.
Right, it’s more complicated than story can show. Chose to focus on evidence of Elwood’s total research, not one experiment.
I disagree with Stelling’s characterization of this being “one experiment.” The entire first paper by Barr and colleagues hinges on the notion that that acids and bases cause crustaceans to groom, and that is indicative of nociception.
Stelling’s answers point out the tension between a good narrative and scientific processes. For a journalistic narrative, uncertainty is uncertainty. There are no need for different gradations of uncertainty. The author of a study going, “It could be something else,” outside experts saying, “ don’t think so,” and sitting down and actually running the entire experiment again and not getting it to work all serve the same purpose in the narrative: saying, “maybe not.”
Scientifically, those forms of uncertainty are not at all equivalent.
Additional, 18 March 2014: Bio News Texas also reports on Crook and Elwood’s work. The article is apparently inspired by, but not a duplicate, of the New Scientist article.
Additional, 25 March 2014: Mike Taylor runs with this, and suggests new kinds of citations.
James Taranto accuses Popular Science magazine of having an agenda in a tweet that expanded into a longer article in the Wall Street Journal. This is relevant to me, because one of the two articles that he mentions is the Popular Science article in which this blog is mentioned.
When Popular Science published the post covering the Nature News article on crustacean pain, around the same time they published an article about the debate over fetal pain.
Elwood “concludes that crustaceans should be protected from the kind of ‘extreme procedures’ they are currently subjected to – things we wouldn’t do to mice, such as lobsters having their legs removed while still alive or crabs being kept tightly bound for days before being sold.”
But McDonough insists no such precautions are due in the case of unborn human beings. Do you think maybe the guys at Popular Science have an agenda?
On the crustacean pain piece, Taranto says the evidence “sounds highly equivocal.” I agree with this. (This is why I like the Popular Science piece: because it does put in caveats like “probably” in the title. I like nuanced reporting.)
The research on crustacean pain is about five years old, and research takes time. If you look at any scientific debate five years in (especially in fields with few labs tackling the problem), it’s likely to sound equivocal.
In contrast, Taranto does not criticize the science reported in the fetal pain piece. I wager that the study of human development, including pain, has been going on considerably longer than five years, and there is probably more confidence about fetal pain than crustacean nociception. Rather than addressing any of the evidence in the piece, Taranto questions the
credibility of the author, calling her a “feminist polemicist.” He suggests the magazine has an
unspecified “agenda.” The suggestion of an “agenda” is strange given that the two articles are by two different authors.
An alternate hypothesis is that the people at Popular Scienceaccurately reported the current state of the science in two distantly related scientific fields. Even if the author lacked credibility and the magazine did have an agenda, that does not automatically make the evidence presented in the articles wrong.
The Nature News blog reports on a recent presentation by Robert Elwood given to the Behaviour 2013 conference about crustacean pain. The headline, as is often the case with headlines, paints a simple picture:
Experiments reveal that crabs and lobsters feel pain
So. We’re done here? Well, no. When you go to the text, you find a more nuanced comment from Elwood:
“Assessing pain is difficult, even within humans,” Elwood told the Newcastle meeting. But there is a “clear, long term motivational change [in these experiments] that is entirely consistent with the idea of pain”.
“Consistent with” is not “revealing.” There can be any large number of hypotheses that can be “consistent with” available evidence, especially when evidence is incomplete or in early stages. If you just had your everyday experience to go by, the sun rising in the East and setting in the West is “consistent with” the Sun going around the Earth (which it doesn’t). It’s also “consistent with” the Earth going around the Sun, and rotating on its axis all the while (which it does).
Elwood appears to have given a review talk of his existing papers on the subject. There are no new data or papers mentioned in the news article. This means that I don’t have to update my previous post on what we know, and don’t know, about crustacean pain. It’s a tricky, tricky subject, and I think it is far too early to call this one definitively yet. Yes, crustaceans may feel pain, but they might not.
This sort of press could have substantial implications for for policy:
Robert Hubrecht, deputy director of the Universities Federation for Animal Welfare (UFAW) and the organizer of the session at which Elwood gave his talk, says that the data for crustaceans appear equivalent to the kind of data that are used to give mice the benefit of the doubt, and thus award them protection from possible pain under the law.
I wonder if Hubrecht has seen any other data besides those generated by Elwood and colleagues. Has there been independent replications of many of these results?
It’s also worth thinking about the consequences if all crustaceans given the same protection as mice. Well, crustaceans are a far more diverse group of animals than mice. Daphnia and Artemia are crustaceans. Daphnia, for example, are barely visible to the naked eye and are used in huge numbers for water quality testing. Some crustacean researchers I’ve talked to dread the effects on those sorts of environmental monitoring efforts if suddenly, a blanket change on regulation to crustaceans were to drop in.
For that matter, why single out crustaceans as special concern? Why not insects, which have as good or better evidence for experiencing pain?
Full disclosure: I have co-authored research in the field of crustacean nociception, which was unable to replicate some early findings.
Additional: See also this post from Magnus Johnson, commenting on the paper that prompted my “What we know (and don’t)” post. I like this piece of writing:
I stand by my feeling that whether animals feel pain or not is irrelevant. To damage or stress a living organisms for no reason other than to enjoy their struggling and suffering is like taking a hammer to a Ferrari or slashing the Mona Lisa. It is an act of pure mindless vandalism.
More additional: Popular Science has picked up this story. This blog makes a cameo appearance in the article.
Additional, 8 August 2013: The Canadian edition of The Huffington Post picks up the story.
More additional, 8 August 2013: I looked at the abstract book for the Behaviour 2013 meeting that Elwood presented his talk at. It’s interesting only one that out of many symposium talks is getting coverage. In the abstract, Elwood puts forward a paper on prawns that was not replicated using three other decapod crustacean species.
Softpedia covers this story as being “as cited in Nature,” which kind of leaves out that this was a conference presentation, not a new paper in the journal.
ZME Science also reports on this Nature News piece.
Additional, 9 August 2013: Nature World News also covers this story. It’s a mash-up the Nature News article and a few other online essays and articles.
If you’re hurt, a physician doesn’t give you an IQ test to figure out how painkiller to prescribe. (“Oh, you knew the meaning of ‘lugubrious’ and solved this trigonometry question? Take another aspirin for that sprain before you go to bed.”) But this is sometimes the approach to determine if we should be worried about caring for animals like this:
This is a squid (Doryteuthis pealeii, formerly known as Loligo pealeii). It’s a cephalopod, related to cuttlefish and octopuses. Anyone who has studied cephalopods is always impressed by how clever they are, which I have documented many times on the blog before. No doubt part of the reason they have big brains is so they can coordinate all the muscles that let them control their colours, like in this video from Michael Bok:
So many people are so impressed with their braininess that, among all the millions of species of invertebrates, cephalopods are routinely singled out as deserving “special consideration” in ethical decisions about their care and use.
But, as I pointed out above, “intelligent” doesn’t necessarily line up in any meaningful way with “pain.” Pain is a hard to get a handle on, scientifically, but a first step to answering whether an animal might experience something like pain is to look for neurons that fire specifically when the tissue is damaged. Neurons tuned to damage are nociceptors.
The quest for nociceptors in the spineless has been incredibly patchy, with very few clear cases until the last decade or so. Despite the amount of interest in the brains of cephalopods, nobody had shown they had nociceptors. That’s where a new paper from Robyn Crook and colleagues come in.
Nociceptors can be tricky to detect using physiology. Their response often overlaps with the responses of other neurons. For instance, high temperatures might fire both regular thermoreceptors and nociceptors. But these two classes of neurons are still different, and convey different information to you. After all, a burn is perceived as more than just high temperature.
One of the common properties of nociceptors is that once active, they work overtime. Repeated stimulation causes greater response in the neurons. For instance, the barest touch a feather, which might have been pleasant normally, can be agony against sunburned skin. Crook and company showed very clearly that there are neurons in the fins of squid that respond to mechanical stimulation that way.
In the top trace below (“pre-crush”), you can see the spikes of sensory neurons that are responding to increasing pressure (red bars; 100 g always damaged the tissue):
After injury (“post crush”), the pressures that originally gave no spikes are responding with big spikes. Pressures that generated spikes before injury are creating even more after injury. This is one of the signs that these neurons are not just touch receptors that respond to pressure, but are nociceptors.
Another feature of nociceptors is that they often (though not always) respond to several different kinds of stimuli. In mammals, nociceptors might respond not only to a pinch, but to high temperatures (usually over 40°C) and acids. The squid nociceptors Crook and colleagues found don’t respond to high temperatures, though no word on other kinds of stimuli. Before you argue, “That makes sense, because squid are aquatic,” trout have nociceptors that are fired by high temperatures (Sneddon et al. 2003).
They also show that these nociceptive neurons become spontaneously active after injury in the whole animal. This is the first time that spontaneous activity of nociceptors has been shown in an invertebrate.
This is an important paper in the study of nociception. And these results are a reminder of the diversity of neural responses. That high temperatures set off our nociceptors does not mean that they do the same in all other species.
Pain is what most people are interested in when they are talking about animal care concerns, but pain is not the same as nociception. Crook and colleagues are (rightfully) cautious about about what their research implies about pain:
Our findings do not directly address the speculation that cephalopods experience pain-like states(.)
These findings don’t answer the question of whether cephalopods feel pain as deeply as a mammal does. It is surely giving us some hints, though.
Full disclosure: I know first author Robyn Crook, having had her as a speaker at a symposium on nociception I co-organized.
Additional: Sea Rotmann asked about how the experiments were done. This is an excellent question. Nociception is related to pain. When you study nociception, you have to give extra thought to whether what you’re doing is needed.
The paper notes that the squid were treated the same way that vertebrates (probably fish) would be. They limited the number of animals used in live experiments, on the assumption that any effects would be large, and made injuries that were smaller than injuries the squid naturally got in their normal routines. Most of the experiments were on isolated fins removed from anaesthetized squid.
All of these say to me that Crook and company exercised due care in they way they carried out their research.
References
Crook RJ, Hanlon RT, Walters ET. 2013. Squid have nociceptors that display widespread long-term sensitization and spontaneous activity after bodily injury. Journal of Neuroscience33(24): 10021-10026. DOI: 10.1523/JNEUROSCI.0646-13.2013
Sneddon LU, Braithwaite VA, Gentle MJ. 2003. Do fishes have nociceptors? Evidence for the evolution of a vertebrate sensory system. Proceedings of the Royal Society B: Biological Sciences270(1520): 1115-1121.
