Lamprey schreckstoff

December 5, 2014 • 5:14 pm

by Matthew Cobb

Take a look at this video, made by researchers at Michigan State University:

These are sea lampreys, an invasive species that has become a real pest in the Great Lakes over recent decades. The substance that is poured into the tank is mushed-up essence of dead lamprey, and it is clearly alarming the fish, to the extent that several of them actually leap out of the tank.

Here’s another view of the same experiment, from under the water:

What’s going on here is both quite amazing, and nothing unusual. The vigour of the lamprey’s response is certainly surprising (the lampreys in particular seem quite astonished!), but this is typical of the response of many fishes to what is termed Schreckstoff.

This fantastic German word – fear stuff, or scary stuff in a loser translation – was coined by Karl von Frisch in the late 1930s. von Frisch is now primarily known for his work on the bee waggle dance – in 1973 he jointly won the Nobel Prize for this work, along with Niko Tinbergen and Konrad Lorenz – but he also studied fish behaviour. As my good friends Marcus Stensmyr and Florian Maderspacher described in 2012:

In the early 1930s, von Frisch was interested in the question of whether fish can hear. He had conditioned a swarm of minnows,a common small freshwater fish, to sounds and wanted to label the conditioned fish: ‘‘To label another member of the shoal, I one day caught a minnow, severed its sympathicus nerve with a thin knife near the end of the tail, which causes a darkening of the skin caudal of the incision site, and set it free. There something unexpected happened: some of the fish became interested in the slightly bleeding wound of the injured comrade and snapped at it; the fish itself retired to the depths and wasn’t seen again; our swarm, however, until then very tame, was now visibly scared and only reluctantly approached the food. About a month later […] one of the minnows was trapped under the edge of the feeding tube. The others regarded the struggling comrade until I liberated it. Now the bad news started spreading through the whole shoal. An increasing unrest took hold, and after a while, half a minute may have passed, they all fled’’.

Von Frisch was intrigued and, passionate enquirer that he was, spent the summer holidays of 1937 further investigating the curious phenomenon. Four years later, he had assembled a 100-page paper concluding: the skin of minnows and other fish harbours a substance — von Frisch called it Schreckstoff (fear or fright stuff) — that is released upon injury and triggers fearful behaviour and escape in conspecifics; the substance is not present in other organs, and is sensed through the nose; skin extracts from one species can sometimes, but not always, induce the fright response in others; a predator attack releases sufficient amounts of Schreckstoffin an injured individual to scare off the swarm.

The nature of this compound, and its significance, has been a matter of debate amongst fish biologists. A number of compounds have been suggested to be involved, in particular hypoxanthine- 3-N-oxide (H3NO), which is found in the mucus of many fish species. In 2012 a study of Schreckstoff in zebrafish showed that two other compounds, complex sugars called chondroitin-4-sulfate and chondroitin-6-sulfate, are involved in this species. In zebrafish, fear tastes sweet.

However, this doesn’t settle the question – what is the point of schreckstoff? Is it an alarm pheromone, or has the response to it simply evolved as a way of detecting whether a fish – virtually any fish – has been injured? If it’s part of a communication system, the sender – the injured fish – has to gain some kind of benefit for the system to have evolved and to be maintained.

In species where the response to danger is to form a shoal, this might be possible, as what Bill Hamilton called the ‘selfish herd’ means that you’re better off together rather than isolated. In this situation, an injured fish would gain benefit from having its conspecifics reduce the chance of it being predated by forming the shoal, while the intact fish would gain benefit by being alerted to the presence of a predator.

But many species do not shoal, and these lampreys certainly show no sign of responding in a coordinated way. In these species, which are probably the majority, it seems that being able to detect schreckstoff is simply a matter of detecting that another fish has been injured, and then finding a way to escape.

One thing that strikes me is that the response of the lampreys, while very robust, is also incredibly short-lived. After 20 seconds or so, they have calmed down. It’s not clear to me what’s going on here.

This video shows why lampreys are a menace in the Great Lakes water system, and how researchers from Michigan State University are using mating pheromones to trap them:

http://www.youtube.com/watch?v=NMutVGTgWC0

This video, from the journal Current Biology, shows how researchers from Singapore discovered the nature of Schreckstoff in zebrafish:

Finally, given that Jerry has acquired a sudden interest in the lives and deaths of English medieval monarchs, it’s only right to note the link between lampreys and Henry 1 (1068-1135), who was King of England from 1100 (he was the fourth song of William the Conqueror and took over after the untimely yet convenient death of his brother William Rufus in a hunting accident). Henry was succeeded by his wife, Matilda, but his nephew Stephen tried to take over, and there was a long period known as The Interregnum in which England descended into civil war. This was only resolved in 1154 when Matilda’s son, Henry II (probably my favourite English king) succeeded Stephen.

Nearly two decades of chaos in England were caused by one thing: lampreys. Henry I, according to the chronicler Henry of Huntingdon, died from eating ‘a surfeit of lampreys’. Henry rejected medical advice, nommed too many of these bizarre jawless vertebrates, and paid the price.

You have been warned.

 

 

Reference: Stenmyr, M and Maderspacher, F (2012) Pheromones: Fish Fear Factor  Current Biology 22:R184-186

41 thoughts on “Lamprey schreckstoff”

  1. I’m amazed at the simplicity and logical nature of this research. It poses and answers questions that surely have wide significance. It should be expanded to mammals (cats?) and then the question of what stimulates human fear responses could be examined.

  3. I just want to point out
    (a) Henry I was succeeded by his daughter Matilda, not his wife (but that’s not that surprising a mistake – his first wife was called Matilda. And his mother. And another daughter outside of marriage. and Stephen’s wife. And his daughter.)

    (b) Everyone’s guide to this (and, indeed, all British history up to WWI) should be 1066 And All That, which tells you all you need to know about Matildas, surfeits and kings, and whether they are Good Things or Bad Things.

  5. If someone dumped a load of mushed-up human beings on me, I’d probably get all excited and run, too! Seriously, I wonder if this would have any relevance to creating an improved shark repellent. There’s an insect repellant technique used in organic gardening: simply collect a cup full of a troublesome insect (bean beetles, potato bugs, etc.), blend them up, and spray the dilute solution on the plants. I used it once with a severe infestation of striped blister beetles on potatoes and they all disappeared within a day!

    3. Maybe this will work for the large numbers of Japanese beetles we get during the late summers. I normally do not go out of my way to crush insects on sight, but regularly I make an exception for them.

      1. Do NOT try this method with Japanese Beetles! When crushed, they give off a smell that actually ATTRACTS more! It is strongly recommended to hand-pick them into a pail of water rather than to crush them.

    4. Wow, that’s where the caterpillars who eat our green beans are going….dust purée and spread on the crops.

    7. It might succeed in creating a shark attractor…
      Shark are usually top predators so if anything I’d imagine they’d be drawn to Schreckstoff, the same way they’re drawn to blood.

      1. That was actually the surfeit of lampreys dude, Henry I. It was the death of his only legitimate son, William in the sinking of the White Ship (real event) that the character Jack’s father survived.

    2. If you can term being drowned in a butt of malmsey (i.e. keg of wine) a “surfeit”. And it wasn’t a king, it was George, Duke of Clarence, brother of Richard III, from the earlier post by Jerry. He would have been king if he hadn’t been murdered first.

  9. I knew this, because of a bit of casual cruelty I remember from college, involving a well-aerated tank of fresh water fish. I don’t know where the idea came from (definitely not from any responsible party), but the “experiment” was to net one of the fish, snap its spine, and toss it back into the tank. Every fish immediately fled to shelter (under rocks, etc). Damn, that’s amazing. Do it again. Ah, the bloody disposition toward natural history.

  10. Matthew

    I’m curious. You said, “If it’s part of a communication system, the sender – the injured fish – has to gain some kind of benefit for the system to have evolved and to be maintained.”

    But what if the “Schreckstoff” was just a natural part of the fish skin, released on injury (like blood), and the evolved trait was the reaction to it. Then, wouldn’t the receiver, an uninjured fish, receive the benefit of the system by fleeing danger?

    2. I think this is what Matthew implied by his subsequent explanation, i.e. it is not actually a communication system but simply evolved detection.

      Unless i misunderstood something, perfectly possible as this is not really my field 😨

    3. I spent some time looking into how ‘communication’, ‘signal’ and related terms are defined in the behaviour literature, and learned that they are highly variable; if anyone uses these terms without giving a specific definition, you have to guess whether it’s meant broadly, narrowly, or in very specific and strange ways. Often too narrowly defined for my taste (can’t see the use of restrictions like ‘has adaptive function X, and evolved specifically to have function X’ in addition to describing what an attribute is observed to do).
      It’s as if engineers hadn’t had a Shannon yet.

    4. Yes! And thus vindicating Edward O. Wilson’s theory of group selection. Take THAT, Dawkins!

  11. I notice my own fish school up if frightened. I think they have it too good in my tank because ones that shoal and school only do so when brought home from the fish store. After that, they go their separate ways.

  12. Neat! I remember seeing on a fishing show (I am a catch and release angler) that a caught fish might freak out others. I wasn’t sure whether or not it was legit, or just speculation.

    Lampreys are indeed a problem. It is not uncommon to catch a trout or salmon in the Great Lakes with lamprey wounds on it.

  13. Fascinating stuff and nothing like the German language to be able to create a pithy yet accurately descriptive word for it.

    Dutch could do “schrikstof”, but that still lacks something IMO.

  14. George C. Williams in his “Natural Selection: Domains, Levels, and Challenges” (1992: pp 113-6) reviews schreckstoff. He points out that the warning signal gives no obvious benefit the fish that is attacked (the substance is released from special cells when the skin is damaged) and that the fish that respond by fleeing or schooling will almost never be close relatives. Gene advantage by individual and kin selection seem to be absent. The fear response seems to be taking advantage of a signal, like blood, in the water. Some researchers proposed that the schreckstoff may be bad tasting (predator may nibble and spit out some prey) or it may help protect damaged skin against pathogens. According to Williams, evidence did not support predator defense. Williams ends by saying that schreckstoff “presents evolutoinary biologists with a serious anomaly.” Apparently it still does.

  15. I’ve never heard of this phenomenon before but it’s really interesting. I had a couple of ideas on how this might benefit the injured
    fish but I’ve no idea if either is near the truth. Firstly if a fish was injured by a predator the scattering effect on surrounding fish could make them more noticeable and attractive to that predator, resulting in the predator being distracted from its original victim. I know from personal experience of fishing that the more noticeable and shiny your lure, the likelier you are to catch a fish. My second thought was regarding the direct effect this might have on a predator – as most predators of fish are other fish is it possible that the effect on surrounding fish also has a repellent effect on some predators? Even a small effect would be highly selective over time. It would be really interesting to douse predators with the ‘essence’ of damaged prey and see what the effect was. Does anyone know if this has been done? I suspect that the effect would be to attract rather than repel predators (as is usually seen in sharks) but it would be interesting to see.

  16. complex sugars called chondroitin-4-sulfate and chondroitin-6-sulfate, are involved in this species. In zebrafish, fear tastes sweet.

    Poetic but untrue. Complex carbohydrates do not taste sweet (just the simple ones). Chondroitin sulfate supplements can be purchased at any healthfood store if anyone would like to taste it for themselves. These are major components of the extracellular matrix of cartilage. Any sufficiently serious injury would put some into general solution.
    If Williams is correct that the stoff is released from cells specialized for that purpose, then there is indeed an evolutionary anomaly here. Is he correct?

Comments are closed.