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Rapid Adaptive Camouflage and Signaling in Cephalopods

Part 1: Concepts and Questions

00:00:01.00 I'm Roger Hanlon, a senior scientist at the Marine Biological Laboratory in Woods Hole.
00:00:04.25 My training is in ethology, or animal behavior, and I am a field researcher, foremost.
00:00:10.23 We also do laboratory experiments and I'll present some of that information to you today on my favorite animal group, the cephalopods.
00:00:17.29 The reason we've chosen this particular subject, signaling and camouflage,
00:00:23.14 is that this is the only animal group on earth that really has these fantastic, unusual and very unique behaviors.
00:00:30.10 So, without further ado, I'd like to really get into the subject right away and introduce this field scene right here,
00:00:37.05 which you'll notice is a little boring, there's just a rock out here,
00:00:41.04 and a lot of sand and a small fish just swimming.
00:00:43.06 And there's really not very much happening in this image for quite a long time until now.
00:00:48.04 You see here this amazing octopus has been on that rock all the time
00:00:52.12 and now it's gone from fully camouflaged to highly conspicuous,
00:00:56.15 swimming away, and you'll watch here, it now spreads its web all over, makes itself look larger than it really is,
00:01:03.04 using high contrast patterning with a large, dark eye, and in reverse, you really get a better feel
00:01:09.19 for the dynamics for what are happening. Watch this ring develop around the eye.
00:01:13.05 That's five million chromatophore organs enervated directly from the brain
00:01:17.16 and now you see the patterning occurring in the skin right here,
00:01:21.04 and then I draw your attention right here, to the smooth outline of the body,
00:01:25.15 and you notice that it goes three dimensional as well.
00:01:28.21 So, in reverse, you really see the dynamics of what's happening and many important features
00:01:35.21 that really represent camouflage in many animals and dynamic camouflage in this one.
00:01:41.05 So, it we look at this carefully, the animal has gone from highly conspicuous
00:01:46.08 to highly camouflaged and in this case, we call this a high fidelity match,
00:01:51.01 which is to say, it looks a lot like the pattern, the posture, the intensity, the color and even the 3-D skin texture
00:01:57.11 of the calcareous algae that's on the rock here.
00:02:00.27 Now, a lot of people think this is what camouflage is, looking exactly like the background,
00:02:05.23 but I want to point out a few features that would bring that idea into question.
00:02:10.28 First I want to point out that right here, if you look in this image,
00:02:15.01 this octopus can go anywhere, on a coral reef or a kelp forest, and camouflage.
00:02:20.23 It doesn't matter if it's a fully developed coral reef, like you see in the top left corner,
00:02:24.24 or anything in between. So, these animals can go where they want, essentially,
00:02:29.04 they can develop the camouflage that's needed for that particular background.
00:02:33.07 So, camouflage is about visual perception. How does the octopus view that background
00:02:40.01 and make this complicated choice? How does the brain control the skin to produce such a diversity of these visual illusions?
00:02:47.05 And, there are many similar questions that one can ask relative to this behavior
00:02:52.21 and that's what I'm going to focus on in this overview of concepts at the beginning.
00:02:57.00 In part two, I will go into more detail about the visual control of this,
00:03:01.23 and in part three, about the skin and the neural control as well.
00:03:04.26 So, we'll look at all facets of this particular behavior.
00:03:07.25 So, this is the burning question that drives a lot of the work in our laboratory
00:03:11.27 and I want to give credit to a very large group of very able collaborators.
00:03:16.05 This is certainly not just my work.
00:03:18.09 Now, I want to introduce the predator. This is a barracuda that one sees on a coral reef,
00:03:24.07 with a fantastic set of eyes, not to mention some pretty good teeth.
00:03:28.17 These animals have superb vision and I want to make this point right now,
00:03:33.08 that, this camouflage system is really tuned to some of the most diverse vision known on this planet.
00:03:40.29 That of teleost fishes, or bony fishes, birds; there are diving birds that go after these animals,
00:03:46.20 and even diving marine mammals. And these are organisms that can see polarized light,
00:03:52.19 they have three or four color receptors compared to our three,
00:03:56.18 some of them can see polarization, many of these predators can see at night,
00:04:01.18 and so there are a lot of attributes of vision that we don't have a humans
00:04:05.25 but this camouflage system has adapted to many of those.
00:04:09.03 So, I want to look at this whole thing as a system really, behavioral ecology is my particular, main field,
00:04:17.22 we're looking at predator-prey relationships, we're looking at communication,
00:04:21.13 we're looking at the theoretical grounds of camouflage which have largely been ignored, as I'll point out soon.
00:04:26.13 It's a study in visual perception, what about the 2D and the 3D objects in the background?
00:04:32.20 There's color, there's texture, there's night, there's motion,
00:04:35.09 there are a lot of things that take into account visual perception.
00:04:38.22 What about the neural control, the motor output of the skin, the optical physics of all this are very important.
00:04:44.19 One has to quantify the light field to know what light is available and then to quantify the light on the animal,
00:04:50.17 to really see how the animal is manipulating the light field through its pattern to avoid predation.
00:04:57.07 Image analysis, quantitatively comparing the animal to its background,
00:05:01.16 is one way that we can measure camouflage.
00:05:03.18 And nanotechnology and materials science have a connection here,
00:05:08.04 biotechnology if you will, because the skin of these animals produces coloration and patterning unmatched to any animal that we know of.
00:05:15.26 And the idea is to see whether some of the principles of operation of the skin
00:05:19.27 can be translated to nanotechnology and meta materials and so forth.
00:05:25.06 And finally, I want to point out art and science.
00:05:27.14 This is all about vision and visual perception and the artistic communities,
00:05:30.28 in the widest sense of the word, really have a lot to contribute to this biological study.
00:05:35.27 So, rapid adaptive coloration is what this animal group does.
00:05:41.22 And I want to point out that the speed of change and the diversity of patterns that these animals have
00:05:48.02 appear to be unmatched of any other animal group we know of.
00:05:52.02 So, we give this a term rapid neural polyphenism. Polyphenism just means many appearances,
00:05:58.04 and each animal can show up to 30 or 50 patterns. That's direct neural control of the skin
00:06:04.20 and again, I emphasize once again, it's attuned to a great many visual systems.
00:06:11.09 So, camouflage is something in which most animals have a fixed pattern or a slowly changing pattern.
00:06:17.12 In that case, the animals have to go to the right place at the right time,
00:06:21.26 right lighting conditions and the right posture to implement their limited camouflage.
00:06:26.24 Changeable patterns, like the cephalopods and many fishes and some reptiles and so forth,
00:06:31.22 can go anywhere and match the background. Therefore, they have a great deal of versatility.
00:06:36.19 So, the slow changing, low diversity animals, pointed out here, reptiles, amphibians,
00:06:42.08 are very different from the animals that change fast and have a lot of diversity.
00:06:47.15 And maybe we can learn something from this group right here that may apply to all the others,
00:06:52.05 that's the direction we're going.
00:06:53.13 So, just a quick word about the cephalopods and why they have such an unusual system.
00:06:58.02 Ancient cephalopods, as depicted over here, really had enormous shells,
00:07:03.24 that's drawn to scale, these are in the fossil record, but through evolutionary time,
00:07:08.07 they went through and lost the shell, achieved buoyancy, locomotion, very complicated brain, wonderful suite of sense organs,
00:07:17.00 and this miraculous skin that we'll talk about in a moment, but the strange thing right here
00:07:22.01 is that they live very fast, they only live for a year or so, they grow very fast,
00:07:26.13 but they have this incredible nervous system, so it's a very unusual life history tactic.
00:07:31.19 A word about art and science. You can see here that we've got a very non-camouflaged cuttlefish,
00:07:37.17 the same animal here, can go very camouflaged and so, if you look at the features that the animals are really dealing with,
00:07:44.19 it really gets down to just five or six features that are being manipulated continually
00:07:49.25 in the skin, in this case. So, these features are things that are shared in art and photography,
00:07:57.00 architecture, landscaping, marketing and advertising and even biotechnology.
00:08:04.01 So, coloration and patterning are all around us. How much do we really understand it?
00:08:08.09 Well, let me go back to zoology for a moment and ask a really rudimentary question
00:08:12.09 and that is, how many camouflage patterns do you think there are?
00:08:15.19 Not just in an octopus or a fish, but any animal, whatsoever. So, this is a question that's hardly been asked before,
00:08:23.17 but I will point out that in our case, we've been studying the cephalopods for a long time
00:08:28.26 and the short answer, we think, is three. Not fifty, five hundred or five thousand,
00:08:34.05 those are answers I typically get when I pose this question. And this is a very unusual, counterintuitive kind of answer.
00:08:41.25 And it's up to me to try and give some data to try and prove that concept.
00:08:46.03 I want to point out however, that even though there are three basic pattern templates,
00:08:50.01 there's a lot of variation on the theme.
00:08:52.09 So, here is a uniform pattern, and we would define this as little to no contrast.
00:08:59.07 I don't care what the color or the brightness is, I'm only interested in little or no contrast,
00:09:05.28 and the same pattern from one end of the animal to the other.
00:09:09.11 Mottled might be described in this case as small scale, light and dark patches of moderate contrast
00:09:18.11 and some general repetition of the pattern.
00:09:20.23 And of course, on a background that has similar features,
00:09:24.06 it would create some nice blending in with the background for camouflage.
00:09:28.06 For disruptive coloration, we now have a very different outlay
00:09:33.27 of large scale, high-contrast light and dark components,
00:09:38.05 multiple orientations and scales, here, partly to break up the recognizable form.
00:09:46.07 But of course, as shown here, on the right background,
00:09:48.21 also creating a fair amount of background matching as well.
00:09:52.16 Now, the idea behind this is that if the cephalopods can go anywhere and hide
00:09:58.14 with only three pattern types, that's a big if, is it possible that maybe all animals
00:10:04.10 have just three or four basic pattern types.
00:10:07.05 And how we arrived at this was to take thousands of pictures of our changeable octopus or cuttlefish
00:10:13.01 and we said, what are we going to do with this mess?
00:10:15.08 You know, is there some sense to this?
00:10:17.01 And we were able to sort of bin it into three or four categories,
00:10:20.23 that's where we came up with this, so the animals are teaching us the answer,
00:10:25.04 we're not dreaming it up sitting at our desk back in the lab.
00:10:28.28 So, with that in mind, I've gone to the trouble, and many of the students in my lab have too,
00:10:34.19 give some examples of uniform patterning.
00:10:37.00 So, we've gone all the way from primates to amphibians to reptiles
00:10:40.29 to fishes to insects and there's a lot of uniform coloration out in the world, we all know that.
00:10:46.06 And on a uniform background, some degree of camouflage will be achieved.
00:10:50.11 Mottled is another kind of general resemblance;
00:10:53.13 again, you see here are birds and other similar groups that I just showed you,
00:10:58.13 doesn't matter if the animals are big or little, or wet or dry, you can find a lot of these coloration types throughout the animal kingdom.
00:11:05.25 And finally, disruptive, which is quite unusual, and exaggerated perhaps the most, in a panda bear or an orca whale.
00:11:16.05 And these are animals, that the refrain here is that there's an enormous amount of bright white and brightness,
00:11:22.19 large-scale, high contrast. And again, in the right background, these can work.
00:11:27.27 Let me give an extreme example. You take a panda bear.
00:11:30.19 Panda bears are sometimes arboreal, if that panda bear is viewed up towards
00:11:35.07 a bright morning, sunlit sky, your retina washes out the brightness, you have deep shadows,
00:11:41.14 and now, this becomes bright sun, this becomes dark shadow,
00:11:46.24 you cannot connect the dots to recognize that that's a bear.
00:11:51.05 So, that's one of the ideas behind disruptive coloration.
00:11:54.15 Now, that said, in the biology circles, the hardest definition we're trying to support among the zoologists
00:12:02.09 is whether or not disruptive coloration really works in that manner.
00:12:06.05 It's hard experimentally to sort that out.
00:12:08.06 The big significance in our view of this is that, if in fact, and it's not fact yet,
00:12:14.21 there are only three camo pattern types,
00:12:17.01 then the implication is that the amazing diversity of visual systems on this planet
00:12:21.13 can be tricked in some degree by just three or four pattern types.
00:12:28.01 So, we need to go some way towards proving that.
00:12:30.11 So, in this publication right here, in 2007, I posited some of these ideas based on our collective work on cephalopods
00:12:38.24 and whether or not this might apply on a larger scale.
00:12:42.16 Well, to say the least, this is a provocative idea, it's been controversial,
00:12:46.09 and I would counter by saying, well, it's testable to some degree.
00:12:51.09 So, I will present some of those tests today, especially in part two.
00:12:54.22 But I'll outline how we go about that now to get the ball rolling.
00:12:57.28 So, back to this fundamental question of what is camouflage?
00:13:02.04 Glibly, I can say that it is probably one of the least studied subjects in biology
00:13:07.03 that we think we already know about.
00:13:08.25 Everyone thinks it's looking just like the background.
00:13:11.10 And I've already hinted that that's probably not what's going on most of the time.
00:13:15.23 I'm going to give an example now of a little more film
00:13:20.23 and this is an octopus on a coral reef, it's moving.
00:13:25.06 Now, movement gives away camouflage, as you well know.
00:13:29.03 And the idea is that when this octopus is foraging, it changes its pattern,
00:13:34.06 we've even measured, about 170 times per hour.
00:13:36.19 So, a search image would not be formed by a predator watching it.
00:13:40.02 See that black and white high contrast?
00:13:42.02 It's very, very easy to see from a great distance, but now, as it gets on this promontory,
00:13:48.06 it stops and settles and puts on this stable pattern.
00:13:52.20 So, I asked a basic question here: does this octopus look exactly like any of these corals that are surrounding it?
00:14:00.26 And I think you'll agree that the answer is no, it doesn't look exactly like any of them.
00:14:04.26 But, it has achieved a really fantastic degree of camouflage.
00:14:08.21 So, to us, this is a far more interesting situation, it's a far more common situation,
00:14:15.01 because coral reefs have hundreds of kinds of corals and algae
00:14:19.19 and sponges and bryozoans and we don't know how many rocks,
00:14:24.17 so, it's not a very sound idea to think that animals would look just like the background to achieve camouflage.
00:14:31.18 So, we can try to push that idea forward,
00:14:35.00 it will help the analysis a little bit. In my view of looking at this,
00:14:39.04 this animal has come up with a generalist solution, a pattern that works
00:14:43.23 to a very complicated visual challenge; what was it looking at in these corals that made it put that particular pattern on?
00:14:51.00 That's really important for us to understand.
00:14:53.21 So, with this idea, we want to move forward and try and analyze the subject a little differently.
00:14:58.15 So, what is camouflage?
00:15:01.02 Background matching, I've already mentioned that, and the first video I showed you was a high-fidelity match,
00:15:06.17 that happened where the octopus looked a lot like the algae.
00:15:09.17 But I've just now shown you the more common case of the generalist match.
00:15:13.11 So, statistically, you cannot find a statistical match, a true one,
00:15:18.17 in any of the camouflage images we have, and we've got tens of thousands of them.
00:15:22.13 So, exact matching is really not the greatest term.
00:15:25.17 Disruptive coloration, which I've also mentioned here, also takes care of some anti-detection,
00:15:33.12 but it disrupts the recognition and this is done partly by these features of internal contrast and edge design,
00:15:40.16 it wants to get rid of its outline edge and mask that, create false edges,
00:15:45.24 so that you don't know where the animal actually is, that's one of the main tricks they use.
00:15:49.26 And masquerade, which has to do with looking other than itself, whatever it is,
00:15:54.29 that might be mimicking another animal or some kind of deceptive resemblance,
00:15:59.06 to a piece of algae or a rock, many animals have tricks like this.
00:16:03.03 Now, I won't pretend to say that all of the camouflage literature can be summed up in these three items,
00:16:07.28 but they are the general ones and I think that you can use these
00:16:12.18 as a way forward if you want to study this subject in a little more detail.
00:16:15.23 What we're after is trying to quantify camouflage and that is a really daunting task
00:16:21.26 and there's no book or paper to go for that.
00:16:24.16 There are a few worthwhile books for those interested,
00:16:27.12 this is the real classic, Hugh Cott, 1940, Adaptive Coloration in Animals, it's really a prescient piece of work,
00:16:36.05 very thoughtful and a lot of the ideas in there are ones that we all pay a lot of attention to today.
00:16:41.19 More recently, 2009, there was an equivalent of a book,
00:16:45.17 numerous articles and philosophical transactions of the Royal Society
00:16:49.09 and then coming out just now this year, in 2011, this book on Animal Camouflage.
00:16:55.00 So, the interested reader can move in that direction. So, let me introduce this jigsaw puzzle
00:17:01.02 that you see on your screen, and I'm going to pull some of these bits together
00:17:06.00 and we're going to build a cuttlefish.
00:17:10.17 Now, that cuttlefish has a disruptive pattern, as you see here,
00:17:14.16 and you see this bright white marking and the head bar and there are about 11 components that the body can be broken into.
00:17:22.00 So, the animal doesn't have an infinite number of things that it can show,
00:17:24.26 it's got X number of building blocks that physiologically it turns on in the skin,
00:17:29.07 and it takes different combinations to create any one pattern.
00:17:33.13 So, that's what you see here. Now, it doesn't look very camouflaged until we put it on the right background.
00:17:38.25 So, we go from this to that,
00:17:41.05 and you can then see some of the magic going on,
00:17:44.10 the actual edge of the animal is quite hard to see,
00:17:48.09 and our eyes are drawn either to the bright white spot or to the sharp edges here.
00:17:52.17 So, these are some of the tricks we think are characteristically happening.
00:17:56.09 Now, the real goal here, for all of us, is to understand camouflage well enough
00:18:03.09 and to understand backgrounds well enough, so that eventually, we can predict,
00:18:07.21 when an animal goes there and stops, it's going to deploy X pattern
00:18:11.22 and to try and do that qualitatively and quantitatively, that's really what we're looking for.
00:18:16.05 Now, we're a long way from that, but we do have a few operating principles that can help us.
00:18:20.26 So, that brings us to this key subject: how does this animal move around, look at this background,
00:18:26.07 and so quickly achieve adaptive coloration?
00:18:29.16 So, experimentally, we're lucky because cuttlefish and octopus are an animal whose primary defense is camouflage.
00:18:38.02 So, they are just genetically driven to camouflage, no matter what background you give them.
00:18:43.14 It's an astounding feature that we can exploit in the laboratory.
00:18:46.18 And the concept that I'm really going to posit to you right now
00:18:50.02 is that if there are only three basic pattern types, then to achieve this fast change,
00:18:56.24 occurring in less than a second, they can't have a brain the size of this room to analyze all that information.
00:19:02.04 We think that they're ignoring a lot of visual information and looking just at one or two
00:19:08.06 key attributes of the background to turn each of the pattern types on.
00:19:12.10 That could account for the speed. So, consider it a working hypothesis.
00:19:16.19 Ok, so the animal's eye is rather unusual. When you look at this eye,
00:19:22.03 if do it in cross section, it looks very much like the cross-section of my eye or your eye,
00:19:26.05 but it's actually arranged very differently.
00:19:29.05 And I will point out, in the brain of this animal, these kidney shaped things on the brain
00:19:34.07 are all optic lobe. In the center part, here, are 20 or 30 other lobes of the brain.
00:19:39.28 This is clearly a visual animal and we don't know exactly what those lobes are doing.
00:19:44.16 So, we have a large, complex eye, huge optic lobes, we have a very keen visual acuity.
00:19:49.18 Curiously, they can see polarized light, we cannot see polarized light, not that many animals can.
00:19:55.28 They can see very well at night, I'll show you some data on that.
00:19:59.10 Yet, curiously, they seem incapable of color vision,
00:20:03.08 which has some ramifications for the idea of color-blind camouflage.
00:20:08.22 Because their predators do see color, for the most part.
00:20:11.10 So, how do they get the color right?
00:20:13.08 Alright, here's the experimental design.
00:20:15.15 So, you see in the top here, we've got environmental information,
00:20:20.15 which we present to the eye of the cuttlefish.
00:20:23.26 And then, because it's genetically driven to display some kind of pattern,
00:20:28.13 we've got our three pattern types right here.
00:20:31.13 And bear with me, let's see if it really is just three pattern types.
00:20:35.07 And the idea is, we put a cuttlefish in a uniform background like this,
00:20:38.20 we give it a non-uniform background like that,
00:20:41.17 and we give it a non-uniform background of different scale and different contrast
00:20:45.22 and the animal has now morphed from uniform to mottled to disruptive.
00:20:48.29 Now, what are the cues there?
00:20:51.01 The cues here are black and white, small scale, moderate contrast.
00:20:56.20 The cues here change by spatial scale and by contrast.
00:21:01.00 What are they really paying attention to?
00:21:04.08 Well, first let me show you a dynamic example of the change on a real substrate,
00:21:08.17 rather than the strange ones I just showed you.
00:21:11.11 So, here's a cuttlefish on a sandy bottom, showing a nice uniform background.
00:21:16.08 And somewhat cruelly, we pull the rug out from under it
00:21:19.09 and it sees this non-uniform background and immediately begins to change its pattern.
00:21:24.24 And it settles, a little upset because we moved it, but you can see it goes into this mottled pattern.
00:21:29.24 It would get rid of that little white square if we gave it just a moment,
00:21:32.27 because that's a disruptive mark, but instead our special, talented, three-handed technician
00:21:38.09 rains in white rocks from heaven and look, the cuttlefish looks at the white rocks,
00:21:43.22 and specially goes over and changes its pattern dramatically into a disruptive pattern.
00:21:49.18 So, I think you can understand, if the animal had stayed here, the camouflage would have been very good.
00:21:55.12 It would have been mottled, on a mottled background and that was effective.
00:21:58.25 But, there seems to priority rule here.
00:22:01.04 When the white rocks showed up, the animal went into disruptive coloration.
00:22:05.11 Eighty percent of the visual field would tell the animal to go mottled,
00:22:09.14 but instead, it took the 20 percent of the information and went disruptive.
00:22:13.23 So, what's going on here? The idea, again, is that we think there're some visual cues here that are simple
00:22:20.01 and we're going to try and sort those out experimentally in part two.
00:22:24.17 Alright, just to change gears, to wrap things up in a little different direction
00:22:30.02 and that is signaling. Signaling is the polar opposite of camouflage.
00:22:34.19 These are high-contrast, unambiguous signals. The sender has to deliver to the receiver
00:22:42.03 an unambiguous signal, and that's the idea with animal communication, all communication for that matter.
00:22:47.08 And they use this for a variety of reasons.
00:22:49.14 What I want to point out in an example here, you can see these two squids,
00:22:53.24 these are Caribbean reef squids, and there's a male on the left and a female on the right.
00:22:59.24 Now, you can see that male is fighting, right here, another male,
00:23:03.27 so they're using their coloration and their patterning to conduct a fight.
00:23:07.01 And the pattern on the bottom of the top animal
00:23:10.01 and the top of the bottom animal are very different.
00:23:12.21 The signal is different to the receiver and the sender depending on their position.
00:23:17.16 So, they will carry on these somewhat gentlemanly fights until someone wins
00:23:21.13 and then the successful male will pair with the female.
00:23:26.00 So, now you see, the male on the left, over here, is showing one pattern to the female
00:23:31.09 and on his other side he's showing a white fighting pattern to any approaching males.
00:23:35.25 So, this is dual signal, simultaneously, and if he shows the white pattern to the female, she's gone.
00:23:41.16 And you see as they change places there, he very casually changed his pattern
00:23:46.03 so he didn't frighten away the female with an aggressive pattern.
00:23:49.21 So, again, visual input is modifying the appearance of the animal
00:23:54.00 here in a very social context.
00:23:56.15 So, put another way, we could say, here you have, right here, fifty million years evidence of the two-faced male.
00:24:06.01 So, let's move on from that and see what else we've got going on here.
00:24:10.10 And I want to talk about the key elements here about vision.
00:24:13.13 To achieve the kind of changes that you're seeing, you need a good visual system
00:24:19.06 and you need the skin to implement that patterning and coloration change.
00:24:24.01 So, here we have another example of a cuttlefish at night
00:24:29.27 and the reason to show this is to show you the details of the skin and how optically malleable the skin is,
00:24:37.11 which is to say that, if you look carefully here, and we'll zoom in a little bit,
00:24:41.00 look at this white spot right here, it gets masked and then it turns on again,
00:24:45.05 you see smooth skin, you see three-dimensional skin, you see transverse bars,
00:24:50.12 you see spots, all of this is like electric skin. Here you have a very subtle change,
00:24:56.27 from a not so strong line to a very strong one, and a very subtle change
00:25:04.22 from brown to a little less brown.
00:25:07.19 And now, watch this false eye spot appear on the back, this is a signal.
00:25:11.03 So, you get the idea that the skin can do a lot of things here and we want to look at that feature
00:25:16.25 in part three in particular.
00:25:19.10 So, some summary thoughts. Coloration and patterning are absolutely wide-spread throughout nature,
00:25:26.10 our entire world is based on coloration and patterning for all visual animals.
00:25:30.13 Rapid adaptive coloration has evolved to an extreme in this animal group.
00:25:36.03 So, the idea is whether or not we can pick up the principles of how they use this system
00:25:41.08 and apply them elsewhere. So, I'd like to point out this nice saying:
00:25:46.05 "Organisms with extreme adaptations like this could reveal general principles."
00:25:51.07 This was a famous saying by August Krogh, a Nobel Laureate in the 1920's.
00:25:56.27 I also want to point out, I really haven't made a point of this,
00:26:01.27 that camouflage is really one of the key evolutionary mechanisms that occur on this planet
00:26:06.20 and there's predator-prey interactions. It's an easy thing for a human to understand
00:26:11.09 because we are visual predators and camouflage is something that we're paying attention to a lot,
00:26:17.02 whether you're a hunter or just admiring nature or you're a biologist.
00:26:21.14 So, the problem is that it is very poorly understood from the visual perspective aspect,
00:26:27.08 as well as the principles involved in how it works, and you get a lot of inappropriate assumptions.
00:26:33.08 So, camouflage offers us this unorthodox way to study visual perception,
00:26:38.13 I'll talk about that in part two coming up, and signaling is the opposite of this,
00:26:43.11 always exploiting the same number of small variables, texture, color, pattern, brightness and so forth.
00:26:49.09 Visual input is really guiding both types of behaviors and that skin is controlled by the brain,
00:26:56.17 I'll talk about that in part three, and I particularly want to point out now, as an overview,
00:27:01.21 that it's pigments and reflectors that create all the changeability in the skin.
00:27:08.04 This is a really important point, many folks will think that maybe it's just some set of pigments,
00:27:13.23 or maybe it's just some set of reflectors
00:27:16.12 in some animals. It's really the combination of the two that sets apart this animal group
00:27:21.01 to give it the spectacularly diverse range of appearances. So, with that, I'd like to close this part one
00:27:30.15 as an overview and having posed a few ideas, and to point out this lovely phrase,
00:27:36.14 by Louis Agassiz that sits in the library of the Marine Biological Laboratory,
00:27:41.02 "Study nature, not books."
00:27:42.14 Thank you and in part two, we will delve into some of the visual mechanisms that really support this system.

Part 2: Exploring Mechanisms of Visual Perception

00:00:01.04 I'm Roger Hanlon, a senior scientist at the Marine Biological Laboratory in Woods Hole.
00:00:05.01 I'm an ethologist, an animal behavior person by training
00:00:10.11 and today I'm going to talk about this particular subject right here, the adaptive coloration that we find in the cephalopods.
00:00:17.00 In part two, we're going to talk about some of the experimental approaches,
00:00:21.07 but I would like to remind those of you who might not have looked at part one
00:00:26.16 that there we covered some of the general concepts of this system,
00:00:29.12 what part it plays in the bigger picture of predator-prey interactions and so forth.
00:00:35.15 So, this is the introduction to what the animals actually do,
00:00:39.28 and how we can experimentally some of the ideas that we presented in part one.
00:00:45.05 So, to begin with, you see this cuttlefish underwater, very bright white, very easy to see,
00:00:51.02 and suddenly, it makes the decision to disappear, if you will, into the sand,
00:00:56.05 and scootches in and it's got the coloration and patterning just right.
00:01:00.01 So, the animal started out like this, so there's a dramatic change in appearance.
00:01:04.29 The idea that we want to investigate is how they do this.
00:01:09.26 And in part one, I also showed this octopus video, that gives the same kind of dynamic.
00:01:15.06 So, how, exactly, do that? In the first part we talked about why they do it,
00:01:20.11 now we're talking about the how questions.
00:01:22.19 So, here're some fundamental questions that I'll be able to address in this short presentation.
00:01:28.02 In terms of the pattern, what elicits each of the three pattern types that the animals are capable of showing for camouflage?
00:01:36.05 And I will reiterate those three pattern types in just a moment.
00:01:39.05 And, do they prefer certain bottom types to settle on,
00:01:43.16 even though they have three patterns, can they really go everywhere and still do the camouflage
00:01:48.23 or do they really go and prefer certain substrates.
00:01:51.24 And what happens when the right eye says to go into one camouflage pattern
00:01:56.19 and the left eye says another? Because these animals have their eyes where our ears are.
00:02:02.11 So, they do not have binocular stereopsis that we have as humans.
00:02:06.21 So, this is another interesting question.
00:02:09.15 And furthermore, there are three-dimensional objects out there in the real world,
00:02:14.05 not just two dimensional backgrounds, that I will present to you also, like a sandy substrate
00:02:18.27 would be the two dimensional background, but a rock nearby or a piece of algae or kelp
00:02:22.28 would be the three dimensional one.
00:02:24.13 How does the animal make the decision of which information to use for its camouflage pattern,
00:02:28.21 very fundamental question.
00:02:30.09 What about camouflage at night?
00:02:32.27 Something we don't think very much about, can they really control these camouflage patterns
00:02:37.24 throughout the night and under dark conditions?
00:02:39.18 That would require them to see in the dark and also, it means that there are some nocturnal predators,
00:02:45.11 and we know there are a lot of nocturnal predators.
00:02:47.21 How is the skin texture controlled? I've also shown in part one, again, the skin of these animals can morph
00:02:56.03 into 3D, it's really a great feature of camouflage. How do they do this?
00:03:00.12 And how is the posture controlled, it makes a big difference what position, standing, arms stretched,
00:03:05.04 arms in, it makes a big difference in terms of camouflage. How they do that, how do they control some of that?
00:03:11.08 And what about this idea of color-blind camouflage? Because, as we illustrated in part one,
00:03:17.10 these animals are color-blind, but their predators are not. And they are able to produce
00:03:22.28 beautifully color-matched patterns for camouflage, yet they themselves cannot see color.
00:03:28.06 So, we'll address that question here. Motion camouflage is another thing,
00:03:31.20 we know as animals move, we have motion detectors built right into our eyes,
00:03:35.19 so how do they protect themselves with camouflage while they're moving? There are a few tricks there.
00:03:40.25 And the other thing is, how do some of their visual predators view this, especially the color patterns,
00:03:46.09 the color aspect of a camouflage pattern, we'll give you a nice recent example of that.
00:03:50.16 So, we'll address all of these questions very quickly, but with some experimental data.
00:03:55.21 So, to reiterate the three pattern types right here, we've got, on the far side, the uniform pattern,
00:04:01.27 means little to no contrast, I don't care what the color or brightness is,
00:04:06.00 the mottled pattern right here, small-scale light and dark splotches of moderate contrast,
00:04:12.09 and some repetition of that pattern,
00:04:14.17 and then this crazy-looking thing here, disruptive, which is characterized by very large scale,
00:04:19.19 even bright white, high-contrast markings, with multiple orientations and scales.
00:04:25.03 And again, the first two operate by looking a lot like the background,
00:04:29.13 resembling features of the background,
00:04:31.18 but this last one not only may give some kind of camouflage in terms of looking a bit like the background,
00:04:39.13 but more importantly, it disrupts the recognizable shape of that animal.
00:04:43.11 So, here is the burning question: how do they so quickly look at a background and deploy the right pattern?
00:04:51.05 And so, we take advantage of a key attribute, these animals have a primary defensive camouflage.
00:04:56.26 They're soft-bodied, everything in the ocean eats them,
00:04:59.12 so they've got to have some trick and camouflage is their trick.
00:05:03.01 Now, since we can give them any visual background and they'll try to camouflage,
00:05:07.16 we can develop a laboratory assay to test what kind of visual information influences the resultant body pattern.
00:05:15.05 So, here's the concept that we are testing.
00:05:17.27 Essentially, if there really are only three basic camouflage patterning templates, as I just pointed out,
00:05:24.20 then maybe there are as few as just three visual sampling rules they need
00:05:29.04 that would allow them to make the decision in seven tenths of a second, which is what they do.
00:05:34.19 Otherwise, to analyze all the visual information available to them in any scene,
00:05:39.01 they'd need a brain as big as this room.
00:05:40.29 And they have a big brain, but it's not that big.
00:05:43.05 So, here is the experimental design.
00:05:46.17 We give the animals visual information, which we can create and control,
00:05:50.21 natural substrates as well as unnatural ones. The animal takes that information into the brain.
00:05:56.13 I can treat the brain as a black box because we can measure what's going in
00:06:01.03 and we can measure what's coming out over here, so temporarily at least,
00:06:05.26 I don't need to know exactly how the brain does that, that's a convenience for me.
00:06:10.01 So, if you can just assume for the moment there really are only three pattern types,
00:06:14.11 let's see what kind of information we can get out of that.
00:06:17.03 We give a cuttlefish a uniform background, it does that.
00:06:20.04 Non-uniform background, does something different,
00:06:22.28 and a non-uniform background of higher contrast and larger size and sharp edges,
00:06:28.11 really forces the animal to morph from uniform to mottle to disruptive.
00:06:34.07 So, what are the key visual cues that the animal is using? There aren't too many things different here
00:06:40.19 over to here, they're both checkerboards, but they're a different size and they're a different contrast
00:06:45.19 and there are a few other features that we've begun to look at in detail.
00:06:49.04 So, our basic approach is to study a range of natural marine patterns,
00:06:53.25 I'm a diving biologist, we photograph and video things underwater,
00:06:57.21 we have a wonderful library of not only cephalopods, but any animal that camouflages,
00:07:03.01 and we can use, you know, those to give us an idea of what the range of natural substrates is,
00:07:08.09 and it's enormous, as you might suspect.
00:07:10.11 We can extract from those, however, and we measure some of the salient background features
00:07:15.20 that we think are driving this camouflage patterning.
00:07:18.29 We can imitate these in their simplest form by making computer generated patterns,
00:07:24.06 just with your home computer, an inkjet printer, we laminate it, put it underwater, put the animals on it,
00:07:29.22 and see how they respond to it.
00:07:31.10 So, here, we can then test multiple computer-generated patterns on many cuttlefish,
00:07:36.16 this is called a psychophysics approach, it's just a fancy word that means
00:07:40.17 that we take one or two visual stimuli, we control the number of variables
00:07:45.03 and we see how they respond to various specific things,
00:07:47.25 even some of them as crazy as a checkerboard.
00:07:50.07 And believe me, there are no checkerboards in the ocean.
00:07:52.12 So, the idea here is that we have developed this very robust bio assay of a living animal,
00:07:59.24 untethered, happy and healthy, we put it in a visual background and we allow it to settle.
00:08:06.19 And here is an example of some of the backgrounds we use and here are more and here are more
00:08:10.23 and we've got hundreds more, we can give them all kinds of backgrounds,
00:08:13.28 but we really only develop these backgrounds when we have a specific question that we'd like to address.
00:08:19.11 So, here is one example, here is the same kind of assay,
00:08:23.22 but in this case, we're going to use some natural materials,
00:08:27.23 and we can take rocks like that and we can add sand until the sand fills in the cracks in between,
00:08:34.20 so that changes the shadows and it changes the sharp edges,
00:08:38.26 to see what effect edges have on the resultant pattern.
00:08:42.18 Or we can go to the psychophysics approach, and we can put in low contrast checkerboards
00:08:47.26 or we can do phase reversals and other tricks to the edges of these checkers
00:08:54.11 or we can make lots of little checkers that together comprise a single checker
00:08:59.27 and we can see how they handle all those because there are many more edges,
00:09:04.15 but do they perceive those as single edges and do all those three patterns look more or less the same
00:09:10.03 to the cuttlefish is a basic question.
00:09:11.25 You know, we know that many of these patterns will result in that kind of pattern,
00:09:16.05 a disruptive pattern, characterized here by this white square, and so, there's on example of how we can approach it.
00:09:23.18 Just to look at one of the three pattern types, in this case disruptive coloration.
00:09:28.04 So, looking at this image right here, if you look at the left image, the animal in the middle is showing a disruptive pattern,
00:09:35.00 and it's also showing a disruptive pattern here, on the checkerboard.
00:09:39.03 So, what are the shared features in those two?
00:09:42.12 And I'll point out right here and here and here, there are these light areas
00:09:47.29 in this immediate vicinity where the cuttlefish can see them,
00:09:51.29 and they're about the same size and contrast as the white square,
00:09:57.11 we call it the white square, it's actually a rectangle, that's a physiological white marking on the animal,
00:10:02.14 they're turning that on, along with other disruptive components,
00:10:05.21 when they see other light objects of about the same size in the background.
00:10:09.26 And that's what's happening over here, in this checkerboard pattern,
00:10:12.26 when that white checker is about the size of the white checker on the animal,
00:10:18.04 then they use that as the signal to turn on disruptive coloration.
00:10:21.23 I want to emphasize that this cuttlefish is not trying to look like a checkerboard.
00:10:26.29 It's using one visual cue to turn on a type of patterning called disruptive coloration.
00:10:34.09 Now, we can test that with natural substrates, as you see here.
00:10:40.15 So, you notice the cuttlefish here, disruptive pattern, disruptive pattern,
00:10:44.27 the white squares still on, so all of these are disruptive patterns,
00:10:48.21 and it turns out that they're in response to these backgrounds here,
00:10:52.18 that have light and dark markings and have some white markings that are about the size of the animal's white square.
00:10:58.29 But in the next three images, the disruptiveness disappears and we can,
00:11:03.20 I'm not going to go into how the axes grade camouflage,
00:11:07.19 but you can read some of our papers later on.
00:11:09.22 But the point is, they've gone from disruptive to not disruptive by getting rid of the objects on the background.
00:11:16.01 So, we tested this a little more thoroughly in the following paradigm,
00:11:20.12 in which we now have just some sandy substrates and we put on, in one,
00:11:25.07 ok, there's only sand here, so the animal's uniform. Here, we have dark rocks on sand
00:11:31.02 and here we have light rocks on sand because over here we had light and dark rocks
00:11:36.06 and we didn't know which color rock or which brightness of rock, was causing the disruptiveness.
00:11:41.05 And in fact, you see the answer rather easily
00:11:45.07 because there's the difference in the threshold over there, and on the right,
00:11:50.02 in the red box, you see the threshold here. Clearly, the animals with the black rock
00:11:55.17 are not showing disruptive, and with the white rock, they are.
00:11:58.29 And I want to point out that the contrast between the black rock and the sand
00:12:04.09 and the white rock and the sand is exactly the same, even though it may not look like it,
00:12:08.08 we measured it with spectrometers. So, this is clear evidence
00:12:11.27 that it is the light object on the background that is driving the disruptive coloration in this case,
00:12:19.23 so there it is.
00:12:21.09 So, we can develop algorithms to look at this in more detail.
00:12:25.04 I'll summarize a large number of experiments very quickly and painlessly for you.
00:12:29.14 And that is that the area of lightness in the background has to be about the same area or size
00:12:35.04 as the animal has on its back.
00:12:37.03 The number and density: you don't need very many white objects in the background to turn on this disruptiveness.
00:12:43.05 It can be anywhere from two or three to a few hundred.
00:12:45.10 We've tested them all.
00:12:46.21 The contrast is very important, it all has to be high contrast in this case
00:12:51.01 because disruptive coloration uses high contrast as part of the visual trickery that's going on.
00:12:57.15 So, I put this little picture right here, that's not a real experiment,
00:13:02.20 we've got two formulas of contrast, there's Weber contrast, there's Michelson contrast,
00:13:08.19 there are several ways to measure contrast in the visual world,
00:13:12.14 and that makes a big difference in how you design your experiment.
00:13:15.11 We're trying to understand visual perception.
00:13:17.11 So, the overall brightness of the background will influence the disruptiveness,
00:13:22.13 the edge characteristics, they have to have sharp edges in the background
00:13:25.11 or they don't pay attention and will not turn on disruptiveness,
00:13:28.21 they have various spatial frequencies, and even the global context,
00:13:32.13 which is to say, if there're a bunch of tiny, little white glops,
00:13:35.25 if they're perceived as a single white blop, about the size of their white square, they'll turn it on too.
00:13:40.13 So, we have done experiments on all of these and it gives us an idea
00:13:45.27 of how the eye is acting as a sensor of a complicated background to come up with one general answer
00:13:52.27 and that is disruptive coloration.
00:13:54.22 There's more work to do on this. I'm not going to present the same kinds of experiments,
00:13:59.16 information we've done on mottled coloration or uniform because I just want to make the point here
00:14:04.27 and not bore you with too many details.
00:14:07.01 So, here is something that is really unusual though.
00:14:10.06 So, up here I've got this word "ontogeny" and the real question is this:
00:14:13.24 if you're a little cuttlefish, the size of my little finger down here when you hatch out,
00:14:17.25 they're looking a certain white object because their white square's little because they're little.
00:14:22.23 What happens when they get this big and this big and this big?
00:14:25.18 Are they always looking for the same size rock in the background?
00:14:28.22 So, we tested this right here and in this case, when the animal is very small,
00:14:33.18 just a centimeter and a half or so in size, we gave it a series of checkerboards,
00:14:39.10 from small squares all the way down to bigger ones at the bottom
00:14:43.02 and then when the animals were a little bigger, ten centimeters,
00:14:45.25 we did the same test and when they got up to nineteen centimeters, we did the same test.
00:14:49.24 We actually did many more, all the way up to full adult size, like this.
00:14:52.23 So, we went from little guys to big guys and the answer turns out, right here,
00:14:59.11 you see in all this images, all the way across, this is the disruptive coloration,
00:15:03.24 is always turned on when the white checkerboard here is about the size of the white square on the animal.
00:15:11.02 So, that's kind of cool, it means that one rule works for all sizes of the animal,
00:15:16.17 but the real question is, how do they relate the size of the white square out there
00:15:23.08 with the white square on their back because they can't see on their back?
00:15:27.13 So, this is not a closed feedback loop.
00:15:30.16 So, this is one of the many mysteries, but the experiments are extremely clean.
00:15:35.00 And so, they can do it, we just aren't smart enough to figure out how.
00:15:38.28 Alright. Here is posing a new question: even though they can show three patterns and go anywhere,
00:15:45.00 do they maybe still have a preference for certain ones?
00:15:48.03 Maybe they're better at disruptiveness and that works better against predators,
00:15:51.27 so they look for backgrounds on which they can be disruptive.
00:15:54.23 This is a question that one might ask. So, we tested this.
00:15:57.17 I will say that the tests are based on a lot of our fieldwork, in which we've spent hundreds,
00:16:03.13 thousands of hours underwater, seeing these animals do their camouflage trick
00:16:08.10 and we've never seen them show a preference, they seem to go absolutely where they're foraging
00:16:13.04 or whatever takes them. Nevertheless, we want to test it in the laboratory.
00:16:16.08 So, up here, we've got two experimental chambers. This one up here shows artificial substrates,
00:16:23.07 like the checkerboards and so forth that I showed you.
00:16:25.16 And then we also did natural substrates.
00:16:27.27 And we put the animal in, right in the middle, in the center channel right here,
00:16:31.27 and then gave it a chance to swim into either of the chambers that they wanted.
00:16:36.00 Here are the experimental results. And over here, on the left, this is for the artificial substrates here,
00:16:43.09 you see, in these numbers here, that they were equally likely to go to any of the backgrounds.
00:16:48.26 They did not prefer any of them. On the natural substrates down here, you get the same thing.
00:16:54.09 You get roughly equal numbers of all substrates.
00:16:57.11 So, this was a statistically sound experimental design and it's clearly showing, at least in the laboratory,
00:17:05.23 no preference whatsoever for different substrates. I will point out that in the one here with the sand,
00:17:12.28 when we gave them real sand, they do prefer to bury a little bit in the sand,
00:17:16.11 so, with some depth to sand, they will prefer that a little bit.
00:17:21.23 But in general, there's very little evidence for preference of backgrounds.
00:17:24.29 The next question is what happens when left eye gets one form of input
00:17:31.12 and the right eye gets another. As I pointed out, their eyes are where our ears are.
00:17:35.09 They don't have stereo vision. So, we created, with the help of a very bright graduate student,
00:17:41.09 this unusual design here, where we took advantage of the cuttlefish's propensity to sit near a wall.
00:17:48.09 So we just converged the two walls so it would back itself into the corner
00:17:53.16 and that way we could then present different visual stimuli to the left and the right eye.
00:17:59.02 So, a very simple ethological observation turns out to be useful in the experiment.
00:18:03.21 And of course, there was a wall in this chamber too, so they had not only the 2D
00:18:08.27 but the wall and the 3D information available to them.
00:18:12.05 So, what happened?
00:18:13.13 Well, when we put the animals in, in this case, right here, on both sides, you know, left side and the right side,
00:18:20.15 it was all uniform, they showed a uniform pattern.
00:18:23.13 When we gave them a small checkerboard and it was uniform
00:18:27.04 they showed mottled and the same with disruptive. So those are our controls.
00:18:30.21 We know that they'll do that.
00:18:32.11 Now, we can measure those patterns, I can't just say, that's mottled or that's disruptive,
00:18:37.29 so we've actually graphed out a lot of these right here,
00:18:40.19 and on point, one down here, that is the type of graph that you get when you measure spatial scale against contrast,
00:18:47.29 that's a uniform pattern.
00:18:49.04 Dot ii is a mottled pattern, which is a characteristic thing and then you get this disruptive pattern,
00:18:55.15 so that represents the three you see at the top here.
00:18:58.06 Now, we give them different information on either side.
00:19:02.01 So, right here we have uniform on one side and big checkers here.
00:19:06.15 Down here we have small checkers and big checkers,
00:19:09.20 and here we have small checkers and we have no checkers at all.
00:19:14.04 So, left eye and right eye are getting very different information in those cases.
00:19:18.23 And those results are shown down here, in the solid lines.
00:19:22.12 And the interesting thing is that they take information from both eyes,
00:19:27.03 they integrate that information and they put on a little bit of a hybrid pattern
00:19:32.05 that incorporates, let's say, in this case, a little bit of disruptiveness with a lot of mottle as well.
00:19:39.04 So, they never, ever put on one thing on one side of the body and one on the other
00:19:44.05 because predators would pick that up visually very easily.
00:19:47.11 So, in fact, what happens is that these cuttlefish are responding to cues
00:19:52.28 from both sides of split substrate, that is, both eyes.
00:19:57.19 This is what brains are for.
00:19:59.18 Alright. Let's move on and talk about a little serendipity.
00:20:07.14 Years ago, we had someone drop a pebble in our tank with our little baby cuttlefish.
00:20:14.02 And it was a joke in the lab because everyone said, well, look at that stupid cuttlefish,
00:20:18.24 he swam away from the wall. Cuttlefish always like to be over against a wall.
00:20:22.29 And he swam all the way out in the middle and sat next to the rock.
00:20:25.09 So, the bad joke in the lab was, stupid cuttlefish.
00:20:29.01 Then, later on in the afternoon, someone said, well, maybe there's something magical about that rock,
00:20:33.09 so we finally did some experiments. What we did was we put a cuttlefish
00:20:38.00 in a sandy substrate, like this, and then we put a rock in there.
00:20:43.12 And when we put the rock in, the cuttlefish swam next to the rock and deployed a disruptive pattern
00:20:48.13 because the whiteness gave it the signal to turn on disruptive coloration.
00:20:52.19 Here, we put the animal on a substrate to let it go mottle.
00:20:56.24 We put the same rock in, all the animals swam over and displayed disruptiveness.
00:21:00.21 We've seen a little of this already, right?
00:21:02.27 And so, obviously, the animals are attracted to the rock
00:21:06.10 and the rock is eliciting a different pattern, again, from 80 or 90 percent of the visual field.
00:21:12.19 So, we did these experiments, sort of the psychophysics approach,
00:21:16.16 by using artificial substrate, there's a uniform background.
00:21:19.21 Now, we put in a cube. That's a three-dimensional cube sitting in there
00:21:23.07 and since the checkerboard's about the same size as the white square on the animal,
00:21:28.19 the animal's putting on a disruptive pattern.
00:21:30.27 Now, we put in small checkers and it goes mottled. We put in the large checker three-dimensional cube,
00:21:38.09 it goes disruptive. Now, we send it to this very difficult, almost psychedelic background
00:21:45.02 of checkers everywhere, it makes a human dizzy to look at that by the way.
00:21:48.08 And the animal puts on this really quite thorough and spectacular disruptive pattern
00:21:53.29 using all eleven components, but now we put in small cube, say, will it go back to the mottled pattern?
00:22:00.08 Goes sits next to it and turns on mottle.
00:22:02.15 So, this would suggest that there's some priority of the three-dimensional object in the background
00:22:08.07 over the two-dimensional flat surface that they're looking at.
00:22:12.06 But, there's a fly in the ointment, which is that this response right here,
00:22:17.08 was not completely robust, it wasn't completely consistent,
00:22:20.23 and it turns out that the contrast between this background and that background
00:22:24.27 can make some difference. So, this is not the cleanest of answers here
00:22:28.21 but the three-dimensionality really is playing some key role in their decision for their pattern.
00:22:34.25 Alright, what about at night?
00:22:36.16 Humans are terrible at night, we don't see almost anything.
00:22:40.08 We're not adapted at night. And the question is, what do these animals do at night?
00:22:44.23 So, in our field work in Australia, this is the giant Australian cuttlefish,
00:22:47.29 it actually gets quite large, these bottom six images show animals in beautiful camouflage throughout the night.
00:22:55.11 So, we published a short paper on that, and the data we got were right here;
00:23:00.13 out of seventy-some animals, they were either in disruptive or mottled, and a few were in uniform,
00:23:05.00 but the point was that in every little microhabitat that the animals were found,
00:23:10.08 they had a beautifully tailored camouflage pattern, suggesting rather strongly
00:23:15.21 that their vision was good at night and that they were using the same rules during the day and at night.
00:23:21.08 Alright, so, that was interesting, but, it also begged a real question:
00:23:27.15 can they actually change at night? Because we did our study at night
00:23:30.13 and just took snapshots, so to speak, of the pattern.
00:23:33.06 So, in a laboratory, we did some experiments and we really tested this.
00:23:37.26 So, if you go from left to right, over here, we're going from different light sources,
00:23:44.02 light all the way down to full darkness.
00:23:47.02 So, this is a stable pattern. So, from three in the afternoon with natural light,
00:23:51.15 starting over here, all the way to seven or eight at night, as the light dims,
00:23:55.23 the animals are maintaining their pattern as darkness comes.
00:23:59.21 So, there's point number one: they're not changing. It still doesn't answer the question we're after.
00:24:03.26 Alright, so, what we did then was late at night, now all these lines here at the bottom represent
00:24:11.15 all that transition from light to dark,
00:24:13.27 and then, in the dark, we switched the pattern dramatically,
00:24:19.07 in this case from a uniform to a disruptive pattern, and the animal immediately switched
00:24:24.07 into a strong disruptive pattern.
00:24:26.15 So, it means that under full darkness, this was 0.003 lux, that's starlight,
00:24:32.18 you and I can't see anything under that light, that looks like pitch dark to us,
00:24:36.26 but the animals can perceive that background and they deploy the new camouflage pattern.
00:24:41.21 And this is just another example from two different backgrounds,
00:24:44.05 when, you know, here's before and here's after they do the switch.
00:24:47.27 So, clearly, they're capable of seeing at night and deploying the different patterns for camouflage under full darkness.
00:24:55.03 And of course, starlight only, maybe you can add maybe some clouds,
00:24:59.03 but that's pretty dark. Moonlit nights, much brighter. So, the next thing to talk about
00:25:05.15 is that three-dimensional morphing skin that you saw earlier in part one.
00:25:10.15 And just to refresh your memory, there's the octopus before and after,
00:25:14.27 get out of the way here, and in between it goes through several stages,
00:25:18.24 of smooth to three-dimensional texture, so that piece of skin there and there and there,
00:25:25.07 are all very different, they go smooth to very, very bumpy.
00:25:28.21 Now, we know that a lot of cephalopods can show these papillae, they're called,
00:25:34.22 there's a lot of variety of these, and they can control all of those,
00:25:38.21 they can go from smooth to all three dimensional, kind of spiky and so forth.
00:25:43.07 And we wanted to do this basic thing, ask whether or not this is driven visually,
00:25:49.08 or, can they touch the bottom, feel how three-dimensional, rough it is,
00:25:54.06 and then change the skin accordingly. So, this is a basic question.
00:25:58.11 So, here's a cuttlefish and Justine Allen led this study and she counted all of the papillae,
00:26:04.27 that was an onerous task to begin with, and then she characterized them all
00:26:10.03 and created the following experiment.
00:26:12.05 She made a real substrate and on that real substrate, the animals had three-dimensional information
00:26:18.21 and they had the tactile information, they could actually touch it, we saw what they did.
00:26:22.14 And the next iteration right here, in this case, we had a piece of glass over the top,
00:26:28.19 so we took away the tactile but we left the three dimensional information.
00:26:32.22 And in the bottom, right here, what we did was we did a photograph of the same background,
00:26:37.18 so we took away the tactile information and we took away the three-dimensional visual information
00:26:43.24 to see what the animals would do.
00:26:45.17 Now, at the bottom, believe it or not, that's a cuttlefish,
00:26:47.17 and it's, we're looking from the side and you can see there are bumps all over the place.
00:26:51.19 Alright, so, here are the results.
00:26:54.09 It doesn't matter whether you use the actual, with the glass or the photograph,
00:27:00.17 in all three conditions, the animals are showing all three pattern types.
00:27:05.16 So, we're getting the same response in all of them.
00:27:09.29 And the real data are shown here.
00:27:14.11 And here you see the layout of, in each of the three conditions, we grade how much of the pattern type there is
00:27:21.28 and it's all the same in all three, but that proved the point of the experiment,
00:27:26.19 that they are using vision, they're not touching the background to get the three-dimensionality,
00:27:30.29 but this was a bit of a surprise because in the disruptive patterns,
00:27:35.29 we're only deploying half the number of papillae,
00:27:39.13 so maybe we learned something from this experiment and that is that disruptive patterns
00:27:44.21 and how they optically deceive a predator may not need or utilize that three-dimensional skin texture.
00:27:51.18 That's just an idea that came out of this experiment.
00:27:55.03 Alright, the next thing was to look at these examples of all the papillae and a big surprise came out of it
00:28:04.03 in terms of neural control of the brain of papillae.
00:28:07.12 It's not like the brain has one motor center and one of set of command neurons
00:28:11.15 and it turns all the papillae on or off, Justine and her colleagues found nine independently controlled sets of papillae in the skin.
00:28:18.15 This is complicated and it also goes to point out that this visual control
00:28:23.12 is complicated and important to really fine-tune the three-dimensionality of the skin
00:28:29.20 in addition to the overall visual patterning that's going on.
00:28:34.09 Ok, a little question that fell out of that is the following thing:
00:28:38.03 I mentioned earlier about eyes where your ears are. So, if you're looking with one eye at something,
00:28:43.13 your three dimensional capability is reduced significantly.
00:28:47.07 And this is what the cuttlefish are doing. So, how might they be looking monocularly
00:28:52.21 at a background, picking up these fine, three-dimensionality in the skin and transferring that into their skin.
00:29:00.07 And this is really quite an unusual capability and we really don't have any good data or ideas on how that works yet.
00:29:08.04 Now, let's take you diving for a minute, this is the giant Australian cuttlefish
00:29:13.04 and you see all this spiky papillae up here on the top and there are small papillae down on the front of the animal.
00:29:19.19 Look at these papillae here, some raise up and they see it, some go down,
00:29:23.29 and you can see that it's changing all the time, from smooth skin to three dimensional;
00:29:29.21 that is a dramatic example of a very large set of papillae. Here you have more examples of it.
00:29:36.07 Just the fine-tuned, up-down and look at the papillae over the eye, here,
00:29:42.05 it's periscoped down right there and you'll see more examples in this video.
00:29:46.21 Watch these, right there, so a lot of these are just showing, here they're going to pop right up in a moment.
00:29:53.08 The animals have beautiful control of these and you notice that this is just not, you know,
00:29:59.01 one simple bump,
00:30:00.15 this is a tri-lobed, flat papillae. And so the musculature in this must be quite interesting.
00:30:08.02 We've not really looked at that until recently and we have graduate students and others looking at that capability.
00:30:15.05 Again, you see the papillae are expressed up, now they go down as the animal moves.
00:30:21.02 Here, we'll see a little more of that, look down on the, sort of the cheek down there, you can see those,
00:30:26.00 so these papillae are positioned to be viewed from the side, from the top,
00:30:29.11 from every direction because predators come from all those directions.
00:30:33.05 Now, again, here in this last bit, you'll see that the papillae are well expressed,
00:30:38.25 and then, the animal moves along, decides not to have rough skin,
00:30:46.06 and has this beautiful, smooth skin. And there's no evidence of the presence of those papillae that you just saw out here.
00:30:53.23 So, we're beginning to look at how these work, and we really can report on that in the future, hopefully.
00:31:00.06 Now, there's another component of camouflage, shown right here.
00:31:04.17 Believe it or not, that's a cuttlefish and instead of just getting down and doing this,
00:31:08.19 it's doing this kind of thing and it's got the arms straight up.
00:31:12.02 And we noticed in the field that when the animals were near three-dimensional structures,
00:31:15.28 they oftentimes would deploy several of their eight arms to create postural camouflage as well.
00:31:22.09 So, we tested out in the laboratory and here we put the animal in the tank
00:31:27.05 and we put a terrible facsimile, a piece of green plastic algae in the tank,
00:31:31.18 and again, the cuttlefish swam from the wall, came all the way over, sat next to it,
00:31:36.19 and raised its arms. So, we did it with a different background, the animal did the same thing,
00:31:41.09 but now we did a photograph, which is a 2 dimensional representation of that vertical object
00:31:47.09 and the animals came all the way across the tank, sat next to it and they put their arms up.
00:31:52.11 Well, we took this to the extreme by putting the animals on these broad stripes
00:31:58.09 and now we have a little ring around here and it's all black.
00:32:02.02 So, the animal is putting on some broad stripes there.
00:32:05.29 Now, on the wall, right here, we're putting these same stripes on the wall
00:32:10.11 and they're going, you know, all the way around, and the animal flattens itself
00:32:13.16 and, here it's pushing its arms way out. Now, we change the pattern on the wall
00:32:18.28 to vertical stripes, notice these are vertical now, not horizontal,
00:32:22.23 and the animal takes its arms and puts them straight up in a line with the stripes.
00:32:28.06 And then we do the following trick, to 45 degrees, and zap, they just lower them right down to 45 degrees.
00:32:35.07 So, we've got visually guided arm postures, here's some real data from the experiments.
00:32:41.12 Again, no stripes whatsoever, the arms are just flat and down,
00:32:46.02 vertical stripes, they raise the arms just a little bit,
00:32:49.07 from the bottom instead of being on the bottom here.
00:32:52.05 We go to 45 degrees and you can see the arm go up right here
00:32:56.05 and then we go to 90 degrees and they go straight up.
00:32:58.25 So, here're some actual data and you can see the plots, really, it's the difference here,
00:33:04.08 and here, that's between horizontal and 45.
00:33:07.29 So, it's quite precise, really, and a little bit surprising that these animals are looking at all these features,
00:33:14.21 including the vertical structures and even getting the relative positioning of the arms to achieve the camouflage that they want.
00:33:22.03 Alright, so, what about this really interesting, vexing question of color-blind camouflage.
00:33:29.16 I've mentioned earlier that camouflage has to be color coordinated
00:33:33.21 because most predators have color vision.
00:33:35.23 However, I'm going to show you experiments here, summarize them, anyway,
00:33:40.25 that indicate that the cuttlefish and the octopus and cephalopods in general are color blind.
00:33:46.03 So, how do they achieve a color match when they can't perceive color.
00:33:50.14 Well, are they really color blind? That's point number one.
00:33:53.24 Here's an example of an octopus sitting out in the ocean somewhere
00:33:58.21 and, where's Waldo, Waldo is right here, that's the octopus and it's not the camo I want you to pay attention to,
00:34:05.21 but the amber coloration is really perfectly matched to that piece of algae that it's sitting on.
00:34:12.27 So, I have many pictures we could show you about this color match and it's really very good,
00:34:17.24 but, what about their ability to see color?
00:34:22.26 So, there's a lot of information indicating that they can't see color.
00:34:27.01 First of all, they're only got one pigment in their eye, we have three,
00:34:31.04 RGB, red, green, blue, all these monitors you're watching are all tuned to RGB
00:34:36.14 for our vision. But these animals don't have red, green and blue, they only have one,
00:34:40.29 it happens to be in the blue-y-green.
00:34:42.19 They only have one cell type, they don't have rods and cones like we do.
00:34:47.19 Physiologically, if you do an electroretinogram and you change wavelength
00:34:53.02 there's no Purkinje shift, as there is in a color-perceiving animal.
00:34:57.22 And the behavioral evidence is really good because if you do an optomotor test,
00:35:03.11 that is, if you put them in this drum and you rotate that drum,
00:35:07.19 the animals will follow that and there'll be vestibulo ocular response
00:35:13.05 but if you put these yellow and purple, or any two colors you want,
00:35:18.17 and you get them exactly the same brightness, so that the only different between them is wavelength or color,
00:35:24.15 the animals do not respond to this whatsoever.
00:35:27.07 So, this is a very powerful behavioral assay.
00:35:30.03 There's some learning experiments that have been done too,
00:35:32.13 the point is, that the published literature gives no clue to the these animals being able to perceive color
00:35:37.22 by standard measures as we know in biology today.
00:35:40.25 Well, so we did the following experiment.
00:35:45.17 We decided to test it again, because we didn't believe it either, even though we'd done some of that work.
00:35:50.15 So, we know, up here, that if you put the cuttlefish on a checkerboard,
00:35:54.28 that they show this disruptive coloration. So, we said, ok, in the black and white world, that's what it looks like to us,
00:36:01.24 this animal only has one visual pigment, it's 492 nanometers, that's roughly this color here,
00:36:08.07 so, we think that this might be more or less how the animal sees, that it might be the black and white,
00:36:13.16 because they only see some shades of green. The point is, they can see that checkerboard,
00:36:18.05 probably, this checkerboard probably looks a bit like that to them,
00:36:20.29 and they turn on this disruptive coloration.
00:36:23.22 So, the experiment is quite different.
00:36:25.19 We're going to create yellow and blue checkers and the question is,
00:36:31.11 does it look like that to them?
00:36:32.26 If we get these really to equal each other exactly in brightness
00:36:38.01 and we did that, we measured it.
00:36:39.18 And the question is, what does that animal do?
00:36:42.09 So, here are all the measurements, and the reason we picked yellow and blue is that right here is 492 nanometers,
00:36:49.15 that's the peak sensitivity of their single visual pigment,
00:36:52.25 so, we went on either side of that, here and there, so we got a maximum overlap.
00:36:57.17 So, we gave them the best possible chance to see these colors, if you will.
00:37:01.11 And we measured these very carefully. As a control, we put an animal on an all-yellow background
00:37:07.01 and it looks uniform, they put on a uniform pattern.
00:37:10.02 All blue background, right here, that looks uniform and they put on uniform,
00:37:15.24 and then we gave them the yellow and blue background and they put on a uniform background.
00:37:20.20 Because clearly, they can't see those checkerboards.
00:37:23.09 So, this was another kind of test that seems compelling, but the vision science community would argue that
00:37:29.27 that's not the most compelling experiment, so we did the following experiment.
00:37:34.10 And that is, up here, you see 16 checkerboards and one of the checkers in each one of these
00:37:40.25 is their primary sensitivity to 492 nanometers.
00:37:45.16 So, we know that that one color, all the way across all 16 here, they have the peak sensitivity to see that
00:37:51.27 and then, starting way over with pure white, all the way over here to black,
00:37:57.25 the other checker ran through 16 grayscales.
00:38:00.07 And here are all the backgrounds and what they really look like.
00:38:03.29 So, the hypothesis was that, was the following.
00:38:07.27 When we start over here, we got the black and green, it's going to be high-contrast,
00:38:13.22 the animal's going to show some disruptiveness. Way over here on the other side,
00:38:17.18 where it's white and green, they'll be able to see that.
00:38:19.28 The idea is that as it converges right into that middle substrate right there is that
00:38:24.27 at some point in time, those two checkers are going to be the same brightness.
00:38:28.28 And when they are, we would predict the animal here is not going to show any disruptiveness.
00:38:34.18 Unless they do have color vision, that would be a different story.
00:38:38.03 So, here are the data. And these really are the data, you see I'm swimming in cuttlefish now,
00:38:44.00 these are the real numbers, and over here, you've got lots of disruptiveness and over here you've got a lot disruptiveness,
00:38:50.23 but right behind me, all right down in here, all the disruptiveness has disappeared.
00:38:56.03 So, we did this to many animals, just wanted to show some raw data in the form of calamari,
00:39:01.10 and here are the real data sets. And so, when everyone brought the data into me the first time,
00:39:07.24 I thought it was a joke, it looked like they got it out of a textbook.
00:39:10.19 It looks too perfect. The idea here is that right in the middle, right at substrate 7, 8 and 9,
00:39:18.03 the animals were showing a minimum, this is a grade of disruptiveness, when they got down here to that middle bit,
00:39:24.02 indeed, like the prediction, they could not see the light and the dark, or the greyscale and the green checker at all
00:39:31.07 and it was a uniform pattern to them. So, this is pretty good information
00:39:35.08 showing that they really are not able to perceive color.
00:39:39.22 They just can't do it. However, let's go back to nature and go diving
00:39:44.17 and here's an octopus perambulating along with a good color match, what we call a living rock trick,
00:39:49.04 notice right here, when it got to the kelp, it went from a mottled to a uniform pattern
00:39:53.29 and the color match to the kelp was extraordinarily good.
00:39:57.04 Now, I've got bright video lights on and to use some sunlight, and I'm going to turn them off,
00:40:01.28 you can see the light dimming there, one side and then the other, so that in the end, under the natural light at 70 feet,
00:40:08.00 which does not have much red in it, the color match is very good.
00:40:12.07 But I even introduced full-spectrum sunlight with my video lights and the color match was still good.
00:40:18.05 So, it's going to be hard to convince me that they don't have some active method
00:40:23.03 of assessing color, so it really begs this interesting question of what they can and can't do.
00:40:29.27 Alright, so, here's the question it begs. Maybe they have light sensors outside of the eye?
00:40:36.24 That's a pretty wild idea. But, we published a short paper on this just a year ago,
00:40:43.27 showing that indeed, if you go searching around, that one retinal pigment,
00:40:50.06 I already told you it was tuned to 492 nanometers, that's a kind of blue-green part of the spectrum,
00:40:54.28 the molecule is actually called opsin, it's an opsin molecule and the gene for that is known.
00:41:01.21 So we did a quick and dirty gene search in the skin of the cuttlefish and, lo and behold, we found it.
00:41:06.25 So, the control was right here in the eye, we took it right out of the retina,
00:41:10.19 and of course there's plenty of opsin there, we know that, and we checked all these other places.
00:41:15.19 And we got a positive hit down here on the fourth arm and we got very positive hits on the ventral mantle,
00:41:21.13 which was a big surprise to us, in fact it's still a big surprise.
00:41:25.05 We don't really know what that means. But we got a lot of negative hits on the dorsal surface here.
00:41:30.12 But eventually, we got a positive here on the fin.
00:41:33.14 So, it shows that the exact same pigment that is helping transduce light in the retina
00:41:41.15 is also out in the skin, so that's a powerful notion, it's a suggestive one only,
00:41:47.11 but we've taken this a little farther and begin to study this. And what we did, in a different organism,
00:41:53.11 that was cuttlefish, this is squid, we did an immunofluorescent stain to that opsin molecule
00:42:00.17 and these little yellow flicks, see all these little yellow blips, here and here,
00:42:04.03 the red arrows are showing some of them. The opsin seems to be distributed throughout the skin
00:42:10.15 where all these small little yellow blips are, but up here, and then also down here,
00:42:17.01 we had this incredible concentration of this molecule showing up.
00:42:22.19 And this happens to be a yellow chromatophore and that's a yellow chromatophore.
00:42:28.11 Now, these animals have yellow, brown and red chromatophores.
00:42:31.27 Only showing up are the yellow chromatophores.
00:42:34.17 So, the idea that you've got a light-sensing molecule concentrated and one of the pigment types
00:42:39.29 that create the skin patterning is very interesting.
00:42:42.07 So, it gives a lead about where to look for this. I can't say anything more about it now,
00:42:46.26 we've just begun to study this in earnest, but stay tuned because it looks as though there might be some light-sensing capability in the skin.
00:42:55.13 Now, that doesn't solve the problem of colorblindness
00:42:58.01 because if you're following me, I've only talked about the same single pigment
00:43:03.17 and you have to have two pigments to discern color.
00:43:07.11 And we, so far, have only one. But at least now we can look for other opsins in the skin tuned to a second wavelength
00:43:14.15 or, it's very interesting here, but it happens to be co-located with a yellow pigment,
00:43:19.10 so now we have a green-sensing molecule and we have a yellow filter, potentially.
00:43:26.24 So, there might be a way that could be a dichromatic way of discriminating a little bit of color.
00:43:32.09 There are a few cases out there in biology similar to that. Anyway, it poses an interesting question
00:43:38.05 and we'll have to see where this takes us.
00:43:40.27 Alright, now I want to switch gears because we're finishing up now, and talk about motion camouflage.
00:43:45.27 Right here, you see an octopus, that is an octopus, believe it or not,
00:43:50.07 sitting on a piece of coral in French Indian Indo Pacific Islands.
00:43:56.15 and the camo is very good. But eventually, animals have to move.
00:44:00.05 They just can't stay still. And so, one way of achieving camouflage when you move
00:44:06.07 is what this animal's going to show you right now.
00:44:09.08 And here you see what we call the moving rock trick.
00:44:14.21 And the case here will be a reef in which the octopus is right here and it's slowly but surely moving away from that rock
00:44:23.02 and notice that it's really holding its posture color and pattern.
00:44:27.18 But notice how slowly it's moving. In fact, it's movement
00:44:31.21 does not stand out from the other movement in the visual background.
00:44:35.13 All these waves generated by the sun and ripple are creating false motion in the background
00:44:40.15 and the animal is moving at a rate that doesn't stand out from that rate of movement.
00:44:45.22 So, it's not setting off the motion detectors in a predator's eyes the way one might interpret that.
00:44:51.29 So, this is really some cognitive action going on in the brain of this animal,
00:44:57.11 it's not only getting its pattern and everything else right for the coral that it came off of,
00:45:02.28 but it's holding itself up in this body and its tippy-toeing across the substrate like this,
00:45:08.07 holding all this still, that's a very athletic move.
00:45:11.10 And, it's gauging its speed according to the light movement in the background.
00:45:16.26 Now, on a calm day or a cloudy day, when you didn't have all this false motion,
00:45:21.09 the animal's taking twenty minutes to cover the same distance that it covered in twenty seconds on this.
00:45:26.03 So, these animals have got some other tricks up their sleeve,
00:45:30.10 again, another good use of a rather large, complicated brain.
00:45:35.07 Alright, so wrap up, the ultimate goal in this sort of work is to try to understand camouflage patterning,
00:45:44.11 the control of that patterning and how it depends on the visual information available to the animal
00:45:50.17 in its immediate surround so that, as in any system in biology or science,
00:45:55.15 if you understand all sides of it, you can begin to predict what the animals are going to do.
00:46:01.13 So, with our algorithms for the three patterns types,
00:46:04.06 we can begin to look at backgrounds a little bit and start to look at the background
00:46:09.04 and think about what is it the animal's looking for, we should be able to get
00:46:12.19 some general prediction about at least what kind of pattern it's going to turn on,
00:46:16.17 uniform, mottled or disruptive. But eventually we have to work out these other aspects
00:46:21.00 of the posture and the fine-tuning of that pattern.
00:46:24.00 So, there're many challenges in front of us, but we've certainly got a new view of it
00:46:28.28 based on the lovely cephalopods giving us the chance to test them in the laboratory.
00:46:33.17 Now, one final thing about predators and how they may look at these patterns.
00:46:38.21 So, if you look at this image right up here, this is taken in the RGB space of a typical camera
00:46:44.25 that we all use and in that case, there's actually a cuttlefish right there
00:46:50.18 and the camouflage is very good. And to give a human a perspective on what that looks like
00:46:54.21 we use the old driver test, the driver's license test that you use
00:46:58.08 and, you know, unless you're color blind, you'll see the number 5 right there,
00:47:02.23 so that's what it would look like in the RGB space. Now, we took these images over here
00:47:08.13 with some very new technology, a hyperspectral camera,
00:47:11.21 hyperspectral imaging. These cameras are new, they're expensive, but they have the beauty
00:47:17.05 that instead of having a camera with only, you know, red, green and blue,
00:47:21.23 with three spectra, we can have hyperspectral and we can have any number of the 300 wavelengths
00:47:30.11 that we can see between 400 and 700 nanometers in the visible range.
00:47:34.03 We can tune those into the camera.
00:47:35.13 So, every pixel in our image now has a hundred or two hundred of the 300 possible colors
00:47:42.03 that are available to our visible range.
00:47:46.07 So, that's what these images are and now what we did is we created
00:47:51.07 two hypothetical predators, one that has a dichromat, two pigments,
00:47:56.02 another one that has three, and then we went here and we gave an impression of what those predators would see
00:48:03.15 in this image given their specific capabilities for color.
00:48:09.01 And you can see the dichromat here did not see, you and I can't see, that number any longer.
00:48:17.01 The trichromat, at least the spectra that we put, you know, the three color sensitivities we picked out,
00:48:23.03 could see the 5, not quite as well as you and I see it on the RGB, but they could see it.
00:48:28.27 So, the point is, with two hypothetical predators, this dichromat, this particular fish,
00:48:34.21 is color-blind to that cuttlefish.
00:48:37.09 It can't see the cuttlefish using the color information only.
00:48:41.01 The cuttlefish is hard to see anyway, but we subtracted out all the color and images and I won't bore you with,
00:48:47.03 and we just, you know, it's just not available to them.
00:48:49.23 So, and of course, a monochromat can't see any of this.
00:48:52.29 So, that was a great new tool that's coming along, which I think will allow us to study this aspect of camouflage
00:48:59.27 much more quantitatively. More importantly, from the sensory biology point of view,
00:49:04.25 we can begin to view the world in the eyes of the predator
00:49:08.11 and this new technology is going to allow us to do that and it's just coming right now in 2011.
00:49:15.12 So, hopefully this will change, ten years from now we'll give you a lot more information.
00:49:19.03 Ok, let me provide a few concluding ideas.
00:49:22.29 This dynamic camouflage obviously is controlled visually.
00:49:26.15 I've given you multiple examples of that.
00:49:28.19 Although the cephalopod eyes kind of look a lot like our eyes, they're really very different
00:49:33.19 by several features. They can't see a lot of the things that we can, like color.
00:49:38.19 But most importantly, I think, is this. We now have what we'll call this fancy term,
00:49:44.04 a visual sensorimotor assay. That is, we have live, healthy, untethered cuttlefish
00:49:49.16 responding to this visual information to see how they turn on their camouflage pattern types.
00:49:54.28 If you're still arguing with me about three basic camouflage pattern types,
00:49:59.28 I will say that after thousands of experiments in the last seven years in our lab,
00:50:04.11 we still have not seen patterns outside of these three or four basic pattern types.
00:50:09.15 So, it's beginning to hold. Nor have we seen it in our extensive fieldwork.
00:50:13.09 Two more points and that is there's a lot of future work still to be done,
00:50:17.27 on this and related systems. I've told you how the basic pattern type is put out there,
00:50:23.08 but we know very little about the fine tuning variations of each of those pattern types.
00:50:28.04 And then finally, there're these really interesting, vexing questions about color-blind camouflage
00:50:33.23 and that 3D skin texture. Those are major challenges to vision research.
00:50:38.18 So, with that, I'd like to close, again, with one of my favorite sayings.
00:50:42.27 It's over the door in the library at the Marine Biological Laboratory
00:50:46.05 and it's been there since the 1890's by then-director or trustee, Louis Agassiz.
00:50:52.24 So, thank you for your attention. In part 3, I will be talking about the skin itself
00:50:59.10 and how the skin actually implements all these optical illusions and that will be the sequel.
00:51:05.25 Thank you very much.

Part 3: Changeable Skin

00:00:01.00 I'm Roger Hanlon, a senior scientist at the Marine Biological Laboratory in Woods Hole.
00:00:05.10 In part one of this series, I talked about some of the concepts and general questions
00:00:10.14 about this subject, signaling and camouflage in cephalopods
00:00:15.00 and laid the groundwork for how this unique capability occurs.
00:00:19.15 In part two, I talked in more detail about the visual control
00:00:23.08 of the multiple patterns that the animals can deploy
00:00:26.15 and here, in part three, I'm going to talk about the skin of these animals
00:00:32.00 that allows the amazing visual diversity that they can produce.
00:00:36.07 I will give some small hints as well about there are some folks in the material science and engineering communities,
00:00:42.13 the nanotechnology world, who are beginning to look at animal systems
00:00:46.22 for some bio-inspired approaches to new kinds of adaptable materials.
00:00:52.03 So, to begin with, you can see right here on the image, I've got some of the typical chromatophore organs
00:00:57.28 in the skin of a cephalopod.
00:00:59.23 These are pigmented organs that I'll describe in detail momentarily,
00:01:03.25 but here, you see this image of blue iridescence and the exact same piece of skin,
00:01:11.15 right there, showing not blue, but sort of a pinkish-red iridescence.
00:01:16.03 Now, this kind of iridescence, this is structural coloration,
00:01:19.24 that means that unlike the pigments, which absorb some light and reflect others,
00:01:26.01 structural coloration devices absorb nothing, they purely reflect light.
00:01:31.22 And in many cases, it's very angle-dependent.
00:01:34.17 So, what's happening here between the blue and the red
00:01:37.11 is that the light has been shifted in direction to give a different coloration.
00:01:42.13 So, these are very different ways of handling light, but I want to make the point
00:01:46.05 right from the beginning that the optical diversity shown by these animals is largely enabled
00:01:55.14 by having structural coloration and pigmentary coloration in multiple layers of the skin.
00:02:01.05 And this is a different way to approach creating materials or anything that has coloration and patterning,
00:02:08.14 and the animal kingdom does a lot of this.
00:02:10.17 So, maybe there's something biology can contribute
00:02:14.09 even to our industrial world.
00:02:16.23 So, without further ado, I want to go and remind ourselves that we're looking at animal patterning.
00:02:24.00 This is the giant Australian cuttlefish. It's not quite as big as that relative to me,
00:02:27.29 but it does get up to about this big, they look like little submarines, very beautiful animals,
00:02:32.10 and this large animal swimming right there can, within a second or two,
00:02:36.29 just descend on the bottom and disappear like this, even when you full-frame it.
00:02:42.07 So, the details of this patterning are very interesting, I covered some of those in part two,
00:02:47.09 but I want to talk about, right now, are the details of the light and dark bits
00:02:52.08 and how they create these different appearances.
00:02:55.27 So, first of all, there are millions of pigment organs, the chromatophores,
00:03:00.12 that are creating this pattern, but there is some iridescence and there's all that whiteness in the skin as well.
00:03:05.22 Where does white come from? White is actually a unification, if you will,
00:03:11.24 of all wavelengths together, that's what white is. So, to create white in the skin
00:03:17.09 means that the animal has to collate all of the available wavelengths in the vicinity
00:03:22.24 and then distribute them out in all directions as white.
00:03:25.24 And we're going to show you how this animal does that.
00:03:29.01 Now, I've already mentioned that there are two systems here,
00:03:32.19 one is the pigmentary color shown in the squid,
00:03:35.14 you can see a lot of the patterning here and elsewhere. These are what we call long wavelengths,
00:03:40.22 your reds and your yellows, it's one side of the spectrum.
00:03:45.02 But how do you get the short end of the spectrum?
00:03:47.08 By the way, these are under active control, I'm going to show you a lot of that in a minute,
00:03:50.26 which just means that all of these pigment armored organs are controlled directly from the brain.
00:03:55.11 to create the patterning. Now, in addition, you have this very important
00:03:59.29 set of structural coloration devices.
00:04:01.28 These create the complementary end of the visible spectrum.
00:04:06.01 The short wavelengths, the blues and the greens, and others, and they create some of the white,
00:04:10.03 here, depending on what it is. So, some of these are actively controlled,
00:04:14.25 but many of them are just sitting in the skin, doing their trick with light.
00:04:19.19 And so, some are actively controlled, some are passive.
00:04:23.24 Both have certain features and advantages or disadvantages.
00:04:27.13 Ok, now, this is from a NOVA special in which you can see the yellow chromatophore,
00:04:34.10 so it's a tight pigment sack, these radial muscles attach to the periphery,
00:04:38.17 and when the muscle contracts, it pulls this out into a disk of color.
00:04:43.02 And when there's no neural signal to the muscle, the muscle relaxes,
00:04:47.16 and boink, it goes back in and you don't see that little point of color.
00:04:51.22 So, you can see the red, the brown, then the yellow chromatophores.
00:04:54.03 Now we go under the skin, they're three layers of chromatophores,
00:04:57.09 and you see this iridescent pink and green and blue and then your white base layer down here.
00:05:02.25 So, collectively, you've got the full spectrum of color right here in this layered skin.
00:05:09.25 And this is not unlike the artist's palette, except that most artists are using mainly pigments.
00:05:17.09 Others use reflectors, these animals are using both.
00:05:20.02 Alright, so we can measure the colors in the skin very carefully with a spectrometer.
00:05:25.19 Here's an example of some chromatophores in the skin.
00:05:30.04 If you look where the arrow is right here, you see a yellow chromatophore
00:05:34.06 and it has opened on top of some blue iridescence.
00:05:37.19 So over here we can measure the chromatophore, the red chromatophore here,
00:05:43.20 the yellow chromatophore there. Oh, I'm sorry, this is the blue iridescence
00:05:47.10 and when it's over the top, this is the measurement you get.
00:05:50.03 So, you get an intermediate color because the light is going through a pigment
00:05:53.26 and it's also reflecting off a reflector
00:05:57.00 and it's coming back through the pigment
00:05:58.14 and that's different from the two independently.
00:06:01.25 So, this is part of the complication, or part of the interesting part of the skin.
00:06:05.17 Here's another example with some different colors,
00:06:07.21 but you can see that we can measure these with precision
00:06:10.18 to see what the interaction is between pigments and reflectors.
00:06:14.10 So, the control of the animal is interesting. Here's a cutaway right here
00:06:20.09 of a squid head. You know, the eye would be right here, but if you remove the eye,
00:06:24.25 you've got a brain. And this number one right here is the optic lobe.
00:06:29.19 The optic lobes are enormous in this animal, it's a very visual animal,
00:06:32.27 and the optic lobes send information down to the main part of the brain, number 2,
00:06:38.13 a set of lobes called the lateral-basal lobes.
00:06:40.23 They integrate the information from the left and right eye
00:06:43.28 and they send information to the lower motor center in the brain,
00:06:47.07 right here, number 3. It's called the posterior chromatophore lobe
00:06:50.23 because it operates all the chromatophores on the posterior part of the body.
00:06:55.09 And there's an anterior chromatophore lobe here, number 3,
00:06:58.23 it operates the millions of chromatophores on the arms.
00:07:02.05 So, you have a hierarchy of control, from the optic lobe to an intermediate brain center
00:07:08.09 coordinating that information and telling the lower motor centers
00:07:12.13 how to control each of the millions of chromatophores that are out there in the periphery.
00:07:16.29 So, yes, this is expensive skin, in the sense that it's highly innovated,
00:07:21.29 it's complicated. But, it gives direct active control of all those little dots in the skin.
00:07:28.12 And from those multiple dots, you create patterning.
00:07:31.16 And let me show you a little bit about how that works.
00:07:34.05 So, here we get an example of a piece of skin on a cuttlefish
00:07:40.03 and this is motor neuron right here that's controlling the chromatophores
00:07:45.02 here, and another motor neuron from the brain that controls all of these chromatophores.
00:07:50.00 And the signal comes from the brain to turn those on, you get this sort of patterning right here.
00:07:55.03 Now, there're an equal number of chromatophores all the way through here.
00:07:58.04 It's just that these are expressed, these are not expressed.
00:08:02.06 So, it's an on or off kind of system and they can turn it on to a greater dimension
00:08:07.11 of the chromatophore or a lesser dimension to make this line darker or lighter.
00:08:13.05 I also point out that the white business underneath, and you can see it in the whole animal right here,
00:08:18.12 has those white reflectors concentrated here,
00:08:21.00 so that they can create a high-contrast zebra pattern
00:08:24.07 for signaling, so the skin is constructed in a very specific way.
00:08:30.02 That area right there that I just highlighted, the areas here, where no neural signal said to turn on,
00:08:36.15 so they're just lying there and they're so little, you don't see them on a gross scale.
00:08:40.20 Now, here's an example of a different part. Right here, you see this spot right here,
00:08:46.12 you can see it expressed down here in the animal,
00:08:49.08 and up here, it's not expressed. And the point is,
00:08:52.16 that each of these chromatophores can be expressed in different parts of the pattern.
00:08:57.11 So, there's very intricate control. Some can be combined with others,
00:09:00.20 or turned on or turned off, in a rather complicated matrix.
00:09:05.04 And then the other thing that can happen is this.
00:09:08.19 I'm going to show a video of this in just a moment, but to set the stage,
00:09:11.11 I have a stimulating electrode here, and there's the same stimulating electrode,
00:09:16.00 and we're looking down in the skin here and putting the electrode directly on one of these white spots.
00:09:21.13 And down here, I'm just moving electrode another millimeter or two over here
00:09:27.04 and in this case, as I move electrode from here to there,
00:09:30.15 you see that the chromatophores in this area, they surround the white bits to enhance them
00:09:36.09 and up here, when you stimulate on there, they mask the adjacent white markings.
00:09:41.27 So, by the simple movement of the stimulating electrode on top of a white spot
00:09:47.06 or to the side of it, you can actually see the distribution of the motor neurons
00:09:51.20 and which pigment chromatophores they control.
00:09:54.23 So, if we look at this in a dynamic sense, alright, here's one of those white spots,
00:10:00.22 so I'm going to be moving the electrode from here to there to there
00:10:05.00 and to there in the following video.
00:10:07.12 And now you're going to see, now I'm here, now I'm there.
00:10:12.03 Now I'm here, now I'm there.
00:10:14.18 And now you can begin to see how it works and you also get this sort of plain, low contrast look
00:10:20.21 a bit like this, and a high contrast look a moment ago when it's in between.
00:10:26.04 So, again, by a somewhat simple mechanism of having the skin structured the right way,
00:10:30.21 and having the control over it, you can take advantage of these passive white markings
00:10:34.26 and you can use the very active pigmentary color to complement it.
00:10:40.14 It's really very beautiful as well.
00:10:43.17 So, what's a chromatophore?
00:10:45.05 A chromatophore is some kind of pigment cell. They occur in many animals
00:10:48.20 and I want to point out that they're totally different structures
00:10:52.18 and the word chromatophore is not appropriate because it means something very different in a vertebrate
00:10:57.16 versus an invertebrate.
00:11:00.03 In fish, you have a fixed cell type, the cell shape never changes.
00:11:04.19 What changes is the distribution; either the pigment granules are condensed in one place
00:11:09.16 or they're distributed throughout the fixed cell.
00:11:12.17 Down here, in the frog or lizard, they have the same thing.
00:11:16.06 A fixed cell, the pigments are either in the bottom and you don't see them
00:11:19.22 or the pigments migrate up here and you do see them.
00:11:22.19 Down here, it's completely different, as I showed you in the animation.
00:11:26.19 You've got a tiny little pigment chamber right there and then the muscles pull it out into a disk of color.
00:11:32.02 Super active kind of process.
00:11:35.07 Ok, so the first two, well, the first one can be, this one can be a little bit fast in fishes,
00:11:40.22 sometimes very fast, this is always a slow process.
00:11:43.27 And down here, when you have direct neuromuscular control,
00:11:47.16 you have extremely fast, fine-tuned precision.
00:11:51.03 Here's what some of these chromatophores look like, you've seen a few of them,
00:11:54.24 some are, you know, yellow, red and brown, the predominant colors.
00:11:57.29 They can go sort of pinkish in different species right there.
00:12:00.28 And now, that organ, and I emphasize this is an organ, there are several cell types here,
00:12:07.18 this is not a single cell. So, at the beginning, you've got pigment granules
00:12:12.02 right here, in the middle, you've got radial muscles down here,
00:12:17.07 they're 18 to 20 radial muscles to pull this out.
00:12:19.15 You've got, sorry, nerve fibers right here that actuate each one of the muscles
00:12:24.27 and then, you've got this clever thing here called a cytoelastic sacculus
00:12:28.29 and that's got the stretchiness that closes the chromatophore when the muscles react.
00:12:33.27 So, this is a complicated organ, we don't know as many details about how it works as we'd like,
00:12:39.21 but we are studying this.
00:12:40.23 But here it is in action, you can see this chromatophore right here,
00:12:45.00 this brown one, opening and closing. You can see the muscles down in here
00:12:48.19 pulling it out. And so there's a yellow chromatophore right there that's opening and closing.
00:12:54.09 This is a preparation, a fixed prep, this is not in the live animal,
00:12:57.28 but you get the idea of how it works.
00:13:00.24 And so, it's pulling in all directions, and if you think about the skin,
00:13:05.17 there are muscles overlapping all over the place, so it gets kind of crowded
00:13:09.19 for the muscles, even, in that skin.
00:13:12.00 Here, I'm going to show a lot of patterning in the skin.
00:13:15.15 And, now, this is a live squid, there's no anesthesia or anything,
00:13:19.23 the animal's sitting down there, very happily. And we're going to use a high-definition video camera
00:13:25.26 to zoom closer and closer into the skin, so you can begin to see a little bit about how it works.
00:13:32.21 So, as we go down in the skin, these chromatophores are expanded, these are not.
00:13:38.05 You can see some of the underlying iridescence, and as we move, you know, posteriorly,
00:13:43.08 to, down the animal, you can see where you can create these transverse bars.
00:13:49.03 I want to point out that all of these chromatophores are actually moving a little bit.
00:13:54.01 They're not actually static all the time.
00:13:56.24 Because on the gross scale, you don't see that, and the nerves don't seem to operate that well.
00:14:02.05 I'm going to speed this up a little bit just so you can see a little more of what's going on.
00:14:07.21 We'll go down the skin a little bit.
00:14:09.24 Now we're going about double speed, all that movement in the background
00:14:14.02 is food thrashing around in the stomach, the animals are translucent.
00:14:17.08 And now you see this bit of patterning right here, and as we zoom in,
00:14:22.18 you begin to see the real details of that patterning.
00:14:26.18 Now, watch carefully, in this image we've gone from patterning and the animals closes some more
00:14:31.14 and suddenly it closes all of them. So, we've created that patterning by opening some and closing others.
00:14:38.02 Very fine precision, very beautiful skin.
00:14:40.25 Now, this is an example right here of squid skin, and the squid skin is what we kind of glibly call
00:14:49.23 "low-resolution skin"; it's kind of like a computer monitor that doesn't have a high resolution.
00:14:55.00 Which is to say that the chromatophores, whether they're closed or whether they're open
00:14:59.21 are far apart and they're very big and they're not very dense per unit area.
00:15:04.01 So, this is a drawing right here of the other two.
00:15:07.12 Down here, you have a cuttlefish with the same scale bar and here, in the cuttlefish,
00:15:13.07 you have hundreds more chromatophores per square millimeter
00:15:16.27 than you do in the case of the squid. So, you can have sort of gross patterning
00:15:21.26 or you can have very fine detailed patterning depending on how big your individual chromatophores are.
00:15:28.17 The structural coloration cells, the iridophores, this is just an example, four examples,
00:15:34.15 of what the iridescence could look like.
00:15:36.15 But I did point out earlier that some of these are passive cells just sitting there,
00:15:40.23 but a few of the structural coloration items, like the iridescence, are active.
00:15:45.13 And here's an example, I'll get out of the way here, of a squid underwater that I filmed.
00:15:50.07 Look at this pink iridescence on the ventral part of the animal,
00:15:54.03 right under here. This is all under control of the animal, so they can create this iridescence
00:15:59.19 for some specific uses, but here you can see how delicate that skin is
00:16:04.25 and how beautiful that iridescence is.
00:16:08.18 Now, how do these things work?
00:16:11.18 I can show you this just in two slides.
00:16:13.23 Essentially, here's a piece of skin, in the non-iridescent state. Here is the exact same piece of skin
00:16:20.06 in the iridescent state. Between here and here we added the neurotransmitter acetylcholine,
00:16:26.00 which also occurs in your body as well.
00:16:28.06 And acetylcholine created iridescence in these cells and if we look at the electron micrograph
00:16:36.15 here is the case when it's not iridescent and whatever this material is,
00:16:41.14 in this platelet, it's dispersed and the light's going straight through it,
00:16:45.23 all the way through, boing. In this case, however, something has condensed,
00:16:50.05 now the light comes down, hits that platelet, and bounces off of it.
00:16:54.02 And that's from the action of the acetylcholine.
00:16:57.21 So, we described that years ago. I will point out right here that this is all, just below that platelet,
00:17:03.29 you can follow this line all the way out, and that's extracellular space,
00:17:07.23 it's actually connected out here. So, the acetylcholine, which is a chemical,
00:17:12.09 is actually getting dispersed throughout the skin and then it diffuses
00:17:16.26 down in between these cells, attaches right onto the cell wall,
00:17:20.03 and changes the platelet to make it iridescent.
00:17:23.04 So, there are two mechanisms going on. The acetylcholine will turn the iridescence, or the reflection, on
00:17:30.27 and number two, it can change the color by adding more acetylcholine, shown here.
00:17:36.24 So, in this case, right here, this is the non-iridescent state, right here.
00:17:42.24 Now it becomes iridescent, of a pink and gold, and when more and more acetylcholine is added,
00:17:49.17 like here, and in here, the colors go to a mix of colors and then they go to your shorter wavelength colors.
00:17:56.01 And they do that by making the reflective platelet goes thick, thinner, thinnest,
00:18:02.11 and the other space goes just the opposite.
00:18:05.11 So, you have high refractive index, low refractive index creating this kind of reflection.
00:18:11.17 Now, the figure at the bottom shows the actual concentrations of acetylcholine
00:18:17.03 for each of those four treatments and you can see, these are physiological quantities of acetylcholine.
00:18:23.03 So, it's a true physiological titer that we're showing here.
00:18:26.15 There's the message: this is chemically tuned color for structural coloration.
00:18:32.12 Very unusual mechanism.
00:18:34.21 Alright. What's really interesting here is that several years ago, Wendy Crookes
00:18:40.03 and Margaret McFall and colleagues published a remarkable paper in Science
00:18:44.12 looking at that material that's reflecting the light and the iridophore.
00:18:48.29 And it turns out to be a protein and it's an unusual protein that they named the reflectins.
00:18:54.04 And aptly named I would say. But the animal world doesn't reflect light with protein,
00:18:58.29 this is a very unusual thing. But this reflective protein has some remarkable qualities,
00:19:06.03 some of which are shown in this very nice paper published in Nature Materials
00:19:10.25 by Rajesh Naik and Ryan Kramer and his colleagues showing that if you take some of this reflectin protein
00:19:19.01 and you make more of it in the laboratory and you spread it out on thin films,
00:19:23.00 these individual protein molecules self-organize into a thin film and reflect light.
00:19:30.13 And this is a really truly remarkable capability.
00:19:33.01 One can now even think about making some reflective material out of this protein.
00:19:37.16 So, it sounds very space-age, as the old term goes,
00:19:41.02 but this is a case where biotechnology is showing us some very interesting features,
00:19:45.11 in this case, coming out of the so-called lowly squid,
00:19:49.04 turning into a possibility of showing us how to makes some very different materials.
00:19:54.13 Ned Thomas and his group at MIT, up in Cambridge, Massachusetts,
00:19:59.24 have also used this idea of how iridophores work to create some of these different photonic gels.
00:20:07.11 And they've published some of this information recently, shown down here,
00:20:11.03 to where you can get some of the electrochemical color tuning
00:20:13.27 that's more or less what the squid is doing too,
00:20:16.15 an electrochemical, electro being neuro releasing some acetylcholine,
00:20:21.19 creating a difference in the dimension of these Bragg reflectors.
00:20:25.03 So, it's really starting to inspire the materials community,
00:20:28.23 and I must say the materials community is asking the biologists some very tough questions about how it all works as well.
00:20:34.06 Beautiful multi-disciplinary enterprise.
00:20:37.11 So, a brief summary of the iridophore story is that some are active and some are passive,
00:20:42.01 the active ones are acetylcholine. There are two mechanisms.
00:20:44.26 One, to become iridescent, the other is to change color and that's chemically.
00:20:48.05 And I hasten to point out that there are no muscles or nerves attached to these cells,
00:20:54.06 so that's really unlike the chromatophores, completely.
00:20:59.06 And what happens is acetylcholine is changing the ultrastructure of this protein,
00:21:04.19 it's changing its conformation. In one, light goes through it, and in another,
00:21:08.00 the light bounces off the individual molecules.
00:21:10.11 So, it's really happening at that molecular or nano-scale.
00:21:14.11 And the molecular switch that's going on in those cells is being worked out by Dan Morris
00:21:19.26 at UC-Santa Barbara and many of his colleagues as well.
00:21:22.17 Again, this is thin-film interference, but there are other optical mechanisms of how the reflection is actually produced.
00:21:29.07 So, just one quick slide to point out that, what do we do with this information?
00:21:34.10 The idea is that this information needs to be modeled according to the spectrometry and the ultrastructure of the skin.
00:21:41.03 Here's one sample publication that we've done, that we can look at the cephalopod skin
00:21:46.06 and we can begin to demonstrate with some real metrics how the light is interacting with the pigments and the reflectors
00:21:53.20 and then you can go off and begin to make materials that may use some of those features.
00:21:58.19 So, the penultimate thing I want to look at are the leucophores.
00:22:02.13 Leucophore means white cell, I already mentioned these earlier,
00:22:06.23 and these are assemblages of spheres mixed with the flat-plate iridophores to create the whiteness.
00:22:12.22 Now, these are passive cells, there are no nerves, no muscles, no chemicals,
00:22:17.27 no nothing. They're sitting there doing this handling of light to create white light in every direction.
00:22:24.23 And we want to look, these are protein molecules too, we don't know exactly what they are,
00:22:29.15 but we're beginning to look into that.
00:22:31.05 So, there's lots of whiteness in the skin,
00:22:33.26 you can see this cuttlefish here has various kinds of whiteness.
00:22:37.15 It's used to mitigate the shadows, for camouflage. It creates maximal tonal contrast,
00:22:43.15 between the light and the dark bits, for disruptive coloration,
00:22:48.04 it even creates the optical illusion of three dimensionality.
00:22:51.28 That's called pictorial relief.
00:22:53.06 And it can act as a white or light base layer upon which all the pigments are laid on top of,
00:22:58.11 as I showed you in the video a few minutes ago.
00:23:00.21 So, here's a video scene showing how white is important in signaling.
00:23:05.20 Here's an octopus in the Caribbean, as I was filming it, it's showing me this remarkable display,
00:23:11.28 standing up on two of its eight arms, and making sure that I see the maximum whiteness
00:23:17.18 and spread of the web and creating that high contrast whiteness with the dark chromatophores
00:23:23.20 to give what we call a deimatic display, that means a threat or startle display.
00:23:28.20 So, white is very important as a signal as well because it creates that high contrast.
00:23:33.21 If we look at a cuttlefish right here, there's the full cuttlefish,
00:23:37.16 and we can go down to the piece of a fin where the white spots are.
00:23:40.20 We look at that white spot in more detail, it looks like that,
00:23:43.25 and then we can look at in a light micrograph and you can see some of these leucophores
00:23:49.16 spread around in here, there're some iridophores as well.
00:23:52.19 Now, we can go down, in even greater detail, down here to a transmission electron micrograph.
00:23:58.09 We blow that up a little bit and now you see these spherical leucosomes
00:24:05.22 and they have the adjacent flat iridophore platelets and they're all co-located
00:24:11.20 and if you look very carefully now, at some of these spheres, you look at them
00:24:16.21 with a transmission electron micrograph, right there, and you see all of these little spheres right here.
00:24:21.19 So, all these little spheres are creating most of the whiteness
00:24:27.01 and we wanted to compare that whiteness in a cuttlefish with this white beetle,
00:24:33.16 which is acknowledged to be able to produce some of the brightest white known in the animal kingdom.
00:24:40.03 A beautiful paper published by Pete Vukusic at Exeter University in England in Science
00:24:45.15 and we decided to compare those.
00:24:47.15 So, Lydia Mathgar, in our lab, did the spectrometry on the leucophores
00:24:52.10 and here you see this flat line at high reflectance, all the way across the visible spectrum.
00:24:58.27 That's true whiteness, when every wavelength is equally shone at a high reflectance.
00:25:04.15 This is really quite remarkable if you show it to an optical physicist.
00:25:08.11 So, moreover, she did something very important right here,
00:25:11.26 she took the light up and down, or all the way around,
00:25:15.21 and no matter which direction you looked at it here, you got this beautiful flat, white line.
00:25:20.03 So, no matter what direction you look at, you're getting beautiful, perfect white.
00:25:23.21 So, here are some of the data comparing the beetle, right here, that's the green line,
00:25:31.02 with the cuttlefish, and this is over right here, from 400 to roughly seven or eight hundred,
00:25:38.24 that's the visible spectrum, and you can see throughout that period,
00:25:42.09 the lines are absolutely flat. Both of them have the same high-degree of reflectance of pure white.
00:25:49.03 However, one's a terrestrial animal, working in the air, and you know,
00:25:54.00 the cuttlefish is a marine animal, working in the water.
00:25:56.21 So, Lydia did the following experiment. She took the cuttlefish skin
00:26:01.23 and she dried it, so got rid of all the moisture, desiccated it,
00:26:05.11 and then she took the beetle and she wet it and got it all wet
00:26:08.20 and she did these tests again.
00:26:10.11 And it turns out that the cuttlefish retains its same capability, wet or dry,
00:26:15.28 to show whiteness in every direction, whereas the beetle lost all of its capability
00:26:20.22 for distributing white light once it got wet.
00:26:23.11 So, they work by a totally different mechanism,
00:26:26.02 both are very efficient, but there's something unusually strange about the cuttlefish,
00:26:30.27 because it works wet or dry. So, I mean, this just opens the door for someone to look at this in a lot more detail.
00:26:37.05 Now, here's a little detail for you, and you can see a scanning electron micrograph
00:26:43.10 of one of those leucophores and right here, you see all these round spheres,
00:26:50.00 you can see them in more detail, co-located with these flat platelets
00:26:55.05 that are very characteristic of the iridophores.
00:26:57.04 So, this combination is very important, but we haven't figured exactly how it works.
00:27:02.02 Here is a close-up of some of the spheres that have the protein in them
00:27:07.01 that create that whiteness. They're all tethered, we've just discovered
00:27:10.23 and so we're just beginning to try to understand what the protein is and what its light-reflective capabilities are.
00:27:17.27 And you can also look at these in a different way, with some confocal microscopy.
00:27:23.02 These are the iridophores right here and here you have the leucophores right here.
00:27:27.00 You can begin to see the 3 dimensionality of it all.
00:27:29.09 And here's a better representation of some of these spheres, the leucophore spheres,
00:27:33.25 in their actual 3-dimensional array. And this is very important for modeling
00:27:39.06 to understand what those dimensions are,
00:27:42.11 not only the various diameters of the round spheres, but how they're organized in three dimensions.
00:27:47.23 So, this work is proceeding now as well.
00:27:50.10 So, the skin papillae, here you see the cuttlefish with the smooth skin
00:27:54.11 and there come the papillae. You already saw that in Part 2.
00:27:57.25 But here's another example just to remind those who haven't reviewed Part 2,
00:28:01.25 that you've got this musculature that is very malleable, if you will, to cause 3D structure in the skin.
00:28:09.17 So, underwater, you can see, here's a small octopus in California and it's not showing camouflage,
00:28:16.03 not showing very much papillae, but as it moves over and settles in the kelp
00:28:21.21 it suddenly looks like this, I don't know if you can see the octopus,
00:28:25.02 but it's actually, all of this is octopus right here
00:28:27.22 and you can see lots of these long tendrils of papillae.
00:28:33.03 Of course, there are lots of tendrils of algae and everything else in the background,
00:28:36.11 so this three dimensionality not only obscures the edges of this animal,
00:28:40.25 but it also blends in with all the other little tendrils.
00:28:44.05 Now, in the close-up, we can take the same species in the lab
00:28:47.16 and now we're looking at a very close-up of the skin, but watch very carefully, about right there,
00:28:52.20 and you can see one of those papillae jump up and now in slow motion,
00:28:56.22 it's going back into the skin, so you can see some of the kinetics.
00:29:00.25 So, now you see that this individual papilla was very, very well controlled.
00:29:06.15 So, we're beginning to look at how the shape deformation occurs, working with some engineers,
00:29:12.24 who can study that, and we're looking at the musculature and the basis of that as well.
00:29:17.19 And of course, as I said in the earlier discussion in Part 2, this is visually driven behavior,
00:29:23.19 so controlled by the brain of the animal.
00:29:26.21 Alright, just one last thing is to look at an octopus. This is a small octopus that mimics flounders or flatfish
00:29:35.23 in the Caribbean, Macrotritopus defilippi, is the name of this creature.
00:29:41.02 It's got these extreme arms and look at this beautiful, fine papillae, all over the skin.
00:29:46.03 And again, they can control that to be perfectly smooth or, this sandy habitat,
00:29:50.29 you can see the animal's all smooth right now, it can change quite a lot.
00:29:55.01 So, in summary, to briefly state what we've talked about today, this transition from biology to inspired materials
00:30:04.19 is well under way after a decade of discussion, there really are some animal models,
00:30:09.01 this is just one example that can inspire different ways to form coloration patterns and even 3D texture.
00:30:16.09 Some remarkable achievements have been made recently,
00:30:19.11 I pointed out one of them with the thin films with the iridophores from the squid.
00:30:24.08 And very different disciplines, this is a highly multi-disciplinary enterprise,
00:30:29.07 biology with materials scientists, optical engineers and so forth, can pose good questions to each other.
00:30:35.18 It's really a stimulating way to look at some of these things.
00:30:38.11 And I'll end this particular talk with a Nobel Laureate phrase, Albert St. Giorgi,
00:30:45.11 "Discovery is to see what everyone has seen, and to think what no one has thought."
00:30:49.20 It's really been an inspiring idea for many generations of MBL scientists and others outside.
00:30:54.20 And finally, again, my favorite saying, it's in the library at the MBL, by Louis Agassiz,
00:31:02.08 in the 1890's, "Study nature, not books."
00:31:04.17 Certainly, that's my excuse to get out in the world and go diving a lot.
00:31:08.03 So thank you for your attention, appreciate it, good luck.

Videos in this Talk
  • Part 1: Concepts and Questions
    Part 1: Concepts and Questions
    Audience:
    • General Public
    • Student
    • Researcher
    • Educators of H. School / Intro Undergrad
    • Educators of Adv. Undergrad / Grad
  • Part 2: Exploring Mechanisms of Visual Perception
    Part 2: Exploring Mechanisms of Visual Perception
    Audience:
    • General Public
    • Student
    • Researcher
    • Educators of H. School / Intro Undergrad
    • Educators of Adv. Undergrad / Grad
  • Part 3: Changeable Skin
    Part 3: Changeable Skin
    Audience:
    • General Public
    • Student
    • Researcher
    • Educators of H. School / Intro Undergrad
    • Educators of Adv. Undergrad / Grad
Speaker: Roger Hanlon
Total Duration: 1:50:41
Recorded: July 2011
All Talks in Ecology

Talk Overview

Hanlon introduces the amazing adaptive coloration of cephalopods. He uses video and still photography to showcase their ability to rapidly change color, pattern and skin texture with fine control and a diversity of appearances, to produce camouflage or to send signals. He argues that all camouflage patterns in nature can be grouped into three types. In part 2, Hanlon shows us results from his lab that make a convincing case that the rapid adaptive coloration of cephalopods is controlled by their visual system; quite impressive for a color-blind animal! Part 3 focuses on the unique skin of cephalopods including the system of pigments and reflectors that allows it to quickly change to any hue and contrast, and the papillae musculature that allows the skin to deform and create multiple 3D textures.

Speaker Bio

Roger Hanlon

Roger Hanlon

Dr. Hanlon’s career path seems to have been determined by fate; as a teenager scuba diving in Panama, he came across an octopus on a coral reef and he has been fascinated with them ever since. Hanlon received his undergraduate degree from Florida State University and his MS and PhD degrees from the University of… Continue Reading

Playlist: Circuits, Learning and Behavior

Related Resources

Hanlon RT. 2007. Cephalopod dynamic camouflage. Current Biology 17: R400-R404.

Hanlon RT, Chiao CC, Mathger LM, Barbosa A, Buresch KC, Chubb C. 2009. Cephalopod dynamic camouflage: bridging the continuum between background matching and disruptive coloration. Philosophical Transactions of the Royal Society B-Biological Sciences 364: 429-437.

Hanlon RT, Chiao CC, Mäthger LM, Buresch KC, Barbosa A, Allen JJ, Siemann L, Chubb C. 2011. Rapid adaptive camouflage in cephalopods. In: Stevens M and Merilaita S, eds. Animal camouflage: mechanisms and functions. Cambridge, U.K.: Cambridge University Press. 145-163.

Mäthger LM, Hanlon RT. 2007. Malleable skin coloration in cephalopods: selective reflectance, transmission and absorbance of light by chromatophores and iridophores. Cell and Tissue Research 329: 179-186.

Mäthger LM, Denton EJ, Marshall NJ, Hanlon RT. 2009. Mechanisms and behavioural functions of structural coloration in cephalopods. Journal of the Royal Society Interface 6 Suppl 2: S149-S163.

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