Extraordinary creatures: mantis shrimp

Tom Cronin, what do you find the most interesting about mantis shrimp physiology?

TC: I think the most interesting thing is simply that they're fascinating. They're animals that if you see one, you want to know more about it. They have a certain behaviour that makes you think that they're aware. They seem curious. They seem to be involved with their environment in a way that you don't see often with invertebrates, their sensory systems are very odd, and their way of catching prey is unique to them. Their visual system is completely unlike that found in any other animal that we know about.

What is so special about the mantis shrimp's visual system?

TC: Well, all eyes are based on two components: an optical system to control the light and a sensory detector that detects the light. That's the way our eyes work. Our optical system is our cornea and our lens, and the sensory system is the photoreceptors or light-sensing cells on the retina. It's sort of the same layout as a camera: the classic example is the camera lens is the optical system and the film or the digital array is the sensory system. A compound eye, like the eyes of mantis shrimp and other arthropods, is totally different. It's made up of 1000s of units, and each unit of the eye has its own optical apparatus and sensor, but each sensor doesn't sense an entire image, it just senses the brightness of light, and the animal builds its image by basically comparing all the sensors together. That seems very strange to us, but our eyes aren't so different. We have 1000s of receptors, and we build that image into a single visual experience. So, it's essentially the same result. In most compound eyes – like you see in a bee or a butterfly – the array is shaped like a sphere. Mantis shrimp eyes are unique. They have eyes with basically two halves that are stuck together, and then in between, there's a third part that's functionally totally different. It's a really strange way to make an eye. It's kind of like having both of our eyes combined into a single eye, but with a new eye right in the middle that's also looking at the same point in space. That means that when a mantis shrimp looks at an object, each eye sees it three times. The top half sees it, the bottom half sees it and the part in the middle sees it at the same time, and then the other eye is doing the same thing. So, it's got six views of an object. The two halves on the top and bottom, are probably used, much like our eyes, to register distance. With our two eyes, we get binocular vision, and we use that to get a sense of how far away things are. Mantis shrimp can do that with one eye, because two parts are doing the same job as our two eyes are. The third part is the part that analyses what it's looking at for its colour, its ultraviolet content and its polarization.

You mentioned that mantis shrimp see polarized light and they see into the ultraviolet spectrum. What do they use that for?

TC: The polarization is useful, because how light is polarized depends a lot on light's interactions with the visual environment. Honeybees use the polarized light pattern in the sky to find their way to a flower patch and to find their way back to the hive. It gives navigational information to them. We have shown that mantis shrimp are the same. They use the sky's polarization as seen through the water surface in shallow water to find their way around and if they're out foraging for food, they obviously have to get back to their burrow. They use polarized light to direct their directions of travel, just like a compass. Also, light underwater is polarized by interacting with water molecules and small particles in suspension. Animals like octopuses – and probably mantis shrimp too – use it to enhance the visibility of objects in the same way that we use polarized sunglasses to enhance the visibility of objects. Also, once you have a polarized light visibility sense, you can also use polarized light for signalling. So, they make signals using polarized light. We wouldn't see those signals as being signals because they don't look special. But to a mantis shrimp, they look unique.

What do you mean by ‘they make signals’?

TC: They build structures in their body covering that manipulate the polarization of light. It sounds exotic, but it's basically the same thing as a bird making a red feather. Well, the mantis shrimp makes a polarized appendage. And just like a colour-blind person can't see the red colour of a red feather, we can't see the polarization signal that mantis shrimp can see. They also make ultraviolet signals. I have a former graduate student, Mike Bok, who's now at Lund University, Sweden, who works on the ultraviolet system. He's shown that in many ways, signals in the ultraviolet range are basically sort of ‘instantaneous messages’. If an animal has a reflection of a particular UV colour, it signals that the animal is aggressive, and it shouldn't be messed with. So, if you show a mantis shrimp that colour of UV, it typically leaves, it won't approach that colour of light. Which is much simpler and more interesting.

Can you describe what cone cells are, and why mantis shrimp have so many?

TC: Well, it's incorrect to call them cones, because cones are the receptors that vertebrates have. Invertebrates, in general, don't have receptors like that. They're evolutionarily totally different. They work utterly differently chemically and electrically than ours do, but they still work on the same principle of catching light and using that light to start electrical signals which then go to the brain. The way we have different colour senses is that we make cones that have different ‘visual pigments’, which are proteins that absorb light and begin the process of creating a signal in the nervous system. Mantis shrimp have the same thing. While they don't have rods and cones, their receptors also have different visual pigments in them. We have three kinds of colour-sensitive cones, whereas mantis shrimp have eight kinds of colour-sensitive photoreceptors. Each receptor is sensitive to one part of the spectrum that they see, and so in the part of the spectrum that we see, which is analysed by one part of this mid band, they would have a violet receptor and then blue/violet, and then blue, and then blue/green, and then green, and then yellow, and then orange and then red. They would have a receptor devoted to each of those individual parts of the colour spectrum, and they somehow pull all that together to get a sense of the colour of something.

Why do they need all these parts to their eyes?

TC: We don't have an answer for that question. It works, and once evolution grabs a hold of something that works, it's kind of hard to throw it away and start over again. The pathway that we imagine happened is that probably at some point, the animals had a sort of elongated eye and it became possible for the two different halves of the eye to see the same thing simultaneously. There are very many crustaceans that have tall eyes shaped like a bean. The only difference with mantis shrimp is that they use the two parts independently and separately, whereas in most animals, it's all one part. But it's not difficult to imagine that at some point it became evolutionarily advantageous to animals that have a sense of distance built into the eye. So that's not a big step from an ancestral crustacean eye. The reason that mantis shrimps might need such an eye is that they catch prey in a way where they smash it or they snare it. To do that effectively, an animal needs to know distance precisely.

Sheila Patek, can you tell us what you think are the most intriguing aspects of mantis shrimp?

SP: The biology of mantis shrimp is just absolutely fascinating in a number of different ways. Obviously, after decades of studying their strike, my answers can relate to that. They evolved mouth parts to be able to perform these incredibly fast strikes and this allows them to spear evasive prey or smash hard-shelled prey. They have evolved different shapes and sizes of these appendages. I love that they're an extremely ancient group of crustaceans, which split off hundreds of millions of years ago from other crustaceans. They evolved all these different capabilities which make them seem very different from other crustaceans.

What types of appendages do they possess? Obviously, there's the clubbing mantis shrimp, are there others?

SP: They have a lot of different appendage morphologies. There are some species that have a more hatchet shape with a spike on the end. Others have a full-blown hammer. Some species have nothing special and just knock limpets off of rocks, as opposed to actually breaking shells. The ‘spearing’ mantis shrimp typically reach out, scoop and then impale their prey on their spines. This is not spearing in the way we typically think of using spears.

Do mantis shrimp use their appendages for anything other than prey capture?

SP: Oh, yeah, absolutely, they're quite multifunctional. For example, the smashing mantis shrimp that we study in Panama live in dead coral rubble. You can find them because they make these absolutely gorgeous little round holes that they hammer just to their size. They also fight with each other. Some species have a specialized tail plate they use as armour. The mantis shrimp hammer back and forth on each other's armor to establish territory or dominance. They probably evolved this armour so that they can resolve conflicts or determine who gets a burrow without a lethal battle.

How hard do they strike?

SP: They can strike with 1000s of times their body weight, which is unimaginable at human scale. Some species use a little hammer that is approximately the mass of two toothpicks, move it at the acceleration of a bullet fired from a gun, and with that, they can break open a snail shell that we'd have to break open with a hammer. It's a difficult question to answer in an intuitive way, because it's not intuitive. If we look at the peak force of a mantis shrimp strike, it's right up there with measurements that people have made by sticking a sensor into the jaws of an alligator or a hyena.

How are mantis shrimp able to generate that much energy with something that has the mass of two toothpicks?

SP: Actually, they use a small amount of energy, on the order of microJoules. Their trick relates to how quickly that small amount of energy is released. This is called mechanical power (power is energy per unit time). They start by loading a stiff spring with a slow, forceful muscle contraction. A series of latches prevents movement of the hammer while the spring is loaded. Then, the latches are removed to allow the spring to propel the hammer rapidly through the water. Again, the duration of energy release is shortened even further because the impact itself is extremely brief – on the order of microseconds. Finally, they cavitate the water, which means that a vapour bubble is formed and then collapses over a nanosecond time period, producing an extreme shockwave. So, it's really about time – shortening the duration of energy release.

What are you hoping to learn about mantis shrimp next?

SP: We are interested in understanding how spring-latch mechanisms allow these animals to be robust to their changing thermal environments due to climate change. We are also interested in their springs: how they are built and how three-dimensional exoskeletal structures can produce an extremely precise output in a very small location. Currently, we're studying how shape and materials distribution have evolved in springs. Geometry is not used a lot in engineering for distributing and focusing energy in elastic mechanisms, but it's what almost all these organisms are doing.

Tom Cronin and Sheila Patek were interviewed by Jarren Kay. The interviews have been edited and condensed with the interviewee's approval.