How to Beat An Octopus at Hide-and-Seek: The Perplexities & Evolution of Cephalopod Camouflage

Paul correctly predicted the results of every 2010 World Cup match that the German team played, including the semi-final game against Spain.

Modern cephalopods rank as the chief intellectual giants of all invertebrates. The 2010 World Cup saw the ascent of Paul the psychic octopus, who predicted the results of Germany’s matches with 100% accuracy. Another charismatic octopus named Otto has put his intelligence to mischief – he resides in an aquarium tank in Germany, and regularly entertains himself by juggling hermit crabs or rearranging the tank furniture. In response to a night lamp that bothered him, Otto discovered that he could direct a stream of water at the light source and short-circuit the electricity. One could write it off as luck, but all other aspects of cephalopod behavior support the notion that modern-day squid, octopuses, and cuttlefish possess some of the most highly developed cognitive capabilities in the animal kingdom. These creatures comprise the subclass Coleoidea, and demonstrate streetwise prey capture techniques, acute dexterity, and intricate communication methods.

Octopus vulgaris shooting ink (Photo from ARKive)

Cephalopods are exclusively marine mollusks that display bilateral body symmetry, a prominent head, large eyes, and arms or tentacles. Most cephalopod species also boast an ink sac that they can use for defense against predators, earning them the common nickname “inkfish” among fishermen. Cephalopods operate on the most complex nervous system among invertebrates. Their intelligence facilitates both top-notch predation and clever predator evasion. While evolution among other classes of mollusks has tended to favor passive defense strategies such as a protective external shell, cephalopods have come to rely on active survival tactics that require wit and intellectual prowess.

This veined octopus has co-opted a coconut shell for shelter (Photo from LA Times)

Advanced cognition and well developed senses support evolutionary innovations that allow cephalopods to successfully eat and avoid being eaten. Octopuses are the only invertebrates that unequivocally demonstrate the capacity to use tools, a behavior that was once considered unique to only humans. They sometimes find abandoned coconut shells and keep them as raw material for creating hiding structures from predators. Furthermore, octopuses in laboratories have demonstrated observational learning, behavior that plenty of mammals don’t even demonstrate. Lastly, perhaps the most important survival tactic employed by modern cephalopods is their unrivaled ability to impersonate another creature or an aspect of their environment. Here I examine the complex mechanisms behind cephalopod camouflage and the evolutionary pathways that transformed cephalopods from defensive, shelled creatures to shrewd masters of disguise.

Squids, octopuses, and cuttlefish are expert hiders. They employ two main mechanistic pathways in concealing themselves. The first involves their ability to modify their appearance physiologically. Cephalopods have “smart skin” that is wired directly to their brains via motor nerves. By coordinating variations of different cell types in their skin, they can create skin patterns that allow them to blend seamlessly into their surroundings. Secondly, cephalopods can hide themselves behaviorally by mimicking the behavior of toxic fish or inanimate objects such as rocks. Their ability to alter both their facade and their behavior presents a double threat and allows cephalopods to fully assume the appearance of the organism or object that they are trying to impersonate, thereby successfully avoiding detection.

Cephalopods employ cryptic coloring for numerous reasons. It allows them to evade predators, deceive competitors, and hunt prey with extra stealth. Color crypsis can also facilitate mating. For example, male cuttlefish often guard a cluster of females as mating partners. To avoid confrontation, another male can disguise its skin to resemble a female cuttlefish and sneak up on a guarded female. Sometimes, this disguise is so convincing that the other male will actually try to guard the intruding male as one of his own females. Cephalopods can also use color changes to communicate with conspecifics, such as by signaling alarm when predators are near or by coordinating swimming patterns within a school. Lastly, the ability to change color can protect a cephalopod from environmental damage. For instance, they can assume darker colors to absorb harmful UV radiation. They can also change their skin color as a thermal buffering mechanism.

Chromatophores (large brown, red and yellow structures) and iridophores (pink iridescent patches) in the skin of the squid Loligo pealeii (image from Lydia Mäthger, MBL)

To witness a cephalopod in the act of assuming cryptic coloration is to witness a miracle of nature. Squid, octopuses, and cuttlefish can change the color and texture of their skin almost instantaneously. The near perfect match and lightning speed of their transformations seem to transcend the realm of the possible. To control the three-dimensional character of their skin, cephalopods use muscles in their dermis that work hydrostatically to create textures ranging from smooth to rough. To accomplish rapid color change, they orchestrate the dual action of chromatophores and structural reflector cells.

Chromatophores are pigment-containing sacs embedded within a layer of the cephalopod’s skin. The organism can produce patterns such as stripes, spots, or bands by differentially expanding or contracting distinct groups of chromatophores. Radial muscles that connect directly to the cephalopod’s brain surround these chromatophore organs. As a result, these color changes occur without synaptic delays, and take place within fractions of a second. Cuttlefish possess up to 200 chromatophores per square millimeter of skin, rendering endless possibilities of combinations to create nuanced patterns and textures.

Iridophores are angle dependent. In squid skin, the same region of iridophores will give off different colors when viewed at different angles. (Photo from Lydia Mäthger, MBL)

To complement the pigment changes of chromatophores, cephalopods also possess structural reflector cells. These include iridophores and leucophores. Iridophores, which are layered beneath the surface chromatophores, contain stacks of thin plates that reflect light. They yield different colors depending on the difference in the refractive index between stacked plates and the spaces between plates, as well as the variable thicknesses of both the plates and spaces. They derive their name from the iridescent hues they create. Iridophores can aid camouflage by complementing chromatophore color changes. Furthermore, studies have shown that squids can increase the spacing between the stacked plates of certain iridophores to allow approximately 90% of incident light to be transmitted through their transparent mantles, thereby minimizing the shadows they cast and rendering them near-invisible to predators viewing them from below.

A blue ringed octopus flashes its blue rings to warn predators of their deadly venom.

In other cases cephalopods may use iridescence to achieve the opposite effect of camouflage and actually make themselves more conspicuous, either to predators or conspecifics. When provoked, the blue-ringed octopus uses its iridophores to flash blue iridescence around the rings on its skin, signaling its deadly venom to potential attackers. Schools of squid also use iridescent stripes to coordinate broad movement patterns. Because the appearance of iridescent patterns differs depending on the orientation from which one is viewing them, neighboring squids within a school can communicate changes in position or swimming direction using stripes that flash when viewed from certain directions.

While iridophores utilize diffraction within their plates to produce color, leucophores, the other type of structural reflector cell, contain organized crystals that reduce diffraction and reflect ambient light. Octopuses and cuttlefish possess leucophores, while squids generally do not. Leucophores are important in creating the bright white color that is the basis of numerous important skin patterns. It provides the background for the zebra-skin displays that male cuttlefish use both to showcase willingness to mate with a female or to signal aggression with another male. White colors are also featured in the designs of fish that octopuses commonly try to impersonate, such as lionfish and banded sea kraits. Furthermore, against a heterogeneous background, bright white patches can serve the important function of distracting a predator from the true outline of a cephalopod.

In addition to transfiguring their skin, cephalopods perform dynamic mimicry as a camouflaging technique. Their ability to do so can be attributed to a highly plastic morphology. Because they are not confined by a rigid internal or external skeleton, cephalopods are extraordinarily flexible. Furthermore, their extensive abilities to convincingly change their skin regime allow cephalopods to take on the patterns of other organisms. Their most obvious impersonations are all of creatures that produce toxins, such as lionfish, flatfish, and sea snakes. This suggests that dynamic mimicry evolved as a mechanism for dissuading predators from attacking. The individual that could learn to imitate new forms of less-impersonated fish species would more successfully elude predators. On an evolutionary time scale, this process would expand the range of configurations that cephalopods could assume. Some scientists believe that, while this behavior emerged as a result of natural selection, it later developed through sexual selection as well. This explanation presumes that male cephalopods would use their ability to change morphologies as a means of impressing females. Females would likely view a broad mimicry repertoire as a sign of fitness, and select for males that had the most persuasive and diverse impersonation skills.

Mimic octopuses impersonating (from top to bottom) a flatfish, lionfish, and sea snake. Octopus on left, actual animal on right.

Along with mimicking toxic organisms, cephalopods also take on forms that allow them to fuse into their surroundings. For example, they can flatten and crinkle their arms and wave them in the current to resemble seaweed. Divers have also observed octopuses assuming the shape of a rock and roving across the seafloor at a slow pace to escape detection. Scientists have deemed this the “moving rock trick” because the octopuses have learned to move at a rate slower than the rate at which the light that penetrates through the water flickers against the seafloor, thus giving off the impression that they are not moving at all.

Primitive cephalopods likely resembled the modern-day nautilus. (Image from National Geographic)

Inevitably, the complexity, precision, and breadth of cephalopod camouflage inspire wonder and curiosity. To better understand how modern cephalopods came to acquire their camouflage capabilities, one must consider the phylogeny and fossil record of cephalopods. Cephalopods emerged from primitive mollusks around 500 million years ago, during the Late Cambrian. They diversified throughout the Ordovician and eventually dominated the Paleozoic and Mesozoic oceans. Primitive cephalopods largely resembled the modern-day nautilus, sporting a thick external shell that provided buoyancy and defense against predators. These cephalopods relied on the siphuncle, a strand of tissue that passed through its shell, to regulate the density of its shell by removing water from its chambers. For these cephalopods, the shell served as a flotation device that allowed them to remain buoyant while conserving energy.

Modern coleoids, which encompass squids, octopuses, and cuttlefish, clearly lack this external shell. Cuttlefish possess an internal shell that still provides buoyancy but no longer serves a protective function. In the squid, the shell has been reduced to a feather-shaped pen that provides structure to its mantle. Modern coleoids also have more developed nervous systems than other mollusks, and are the only two-gilled, or dibranchiate, cephalopods. The only other living cephalopods, nautiluses, are often considered “living fossils” because they still possess an external shell and a tetrabranchiate body plan with an extra pair of gills. Nautiluses also have several undifferentiated tentacles, less developed eyes, and slower response times to stimuli. Thus, more derived cephalopods such as the modern coleoids seem to have evolved towards a mobile, predatory lifestyle that relies on active swimming rather than neutral buoyancy.

Coleoid fossils are relatively rare because ancestors of octopuses, squid, and cuttlefish most likely lacked hard external shells and inhabited the deep sea.

The fossil record provides some insight into this evolutionary process. Unfortunately, cephalopods without calcified shells are also those less likely to remain preserved as fossils. Octopus fossils are relatively scarce and include only a few body specimens. Squid bodies are slightly less perishable, and thus squid fossils are somewhat more abundant, particularly from the Jurassic. Still, because most squids and octopuses probably historically inhabited deep-sea environments, it is less likely that they were preserved in fossils on land, which are far more accessible to paleontologists than deep-sea fossils. Because the fossil record for cephalopods is patchy and likely biased, the story behind the evolution of modern coleoids is largely derived from deductive speculation.

There are several interpretations of how squids, octopuses, and cuttlefish lost their shells. Early on, shelled cephalopods that inhabited shallow waters may have been driven into the deep sea due to competitive pressure from fish or a reduction in shallow marine environments during the breakup of Pangea. An external shell would likely have proven troublesome in deep waters where gas-filled shells could have imploded or high water pressure could have prevented gases from diffusing into shell chambers fast enough. These reasons probably also explain why deep-sea fish often lack swim bladders. Another explanation posits that cephalopods inhabited the seafloor and relied on crawling and burrowing rather than swimming. These bottom-dwelling cephalopods would have no particular use for a buoyant shell – in fact a large external shell may have even proven cumbersome when burrowing. Lastly, coleoids may have lost their external shell in response to predation from echolocating creatures such as dolphins. Hollow shells would yield loud echoes and give away the position of a cephalopod bearing an external, gas-filled shell. This explanation corresponds with the observation that the abundance of cephalopods with external chambered shells declined after the proliferation of echolocating cetaceans during the Miocene.

Without a protective external shell, these creatures had to rely on other predator avoidance tactics such as increased speed, maneuverability, navigation skills, and camouflage ability. Dynamic mimicry suggests that impersonation behaviors evolved as a predator defense mechanism.

Roger Hanlon found and colleagues found that giant Australian cuttlefish perform night camouflage on rock reefs.

Another aspect of cephalopod camouflage that points to predation pressures as the selecting force for camouflage is some cephalopods’ ability to camouflage at night. Roger Hanlon, from Woods Hole Marine Biological Laboratory, recently observed cuttlefish at a spawning ground during the night and found that once night fell, almost all of the cuttlefish became sessile and assumed the appearance of the substrate on which they settled. In fact, 86% of cuttlefish employed camouflage at night compared to a mere 3% during the daytime. This behavior suggests that predation pressures soar high at night, most likely from nocturnal hunters such as seals, bottlenose dolphins, snappers, and mulloway.

Night-time camouflage also provides an idea of the high visual acuity of both cuttlefish and their predators. Cuttlefish vision at night must be well-developed because camouflage requires relatively high-resolution visual cues from the surrounding environment. Meanwhile, the diversity of camouflage patterns that the cuttlefish employed also implies that predator night-time vision is equally keen. In other words, predators must see well enough to detect slight differences between the camouflaged cuttlefish and the seafloor substrate.

Cuttlefish may rely on contrast rather than color to camouflage themselves. (Lydia Mäthger, MBL)

Another curious aspect of cephalopod camouflage suggests that it possibly evolved in response to the cephalopod’s natural environment rather than its predation pressures. While night-time camouflage confirms cephalophods’ high visual acuity, laboratory tests have demonstrated one component of visual perception that cephalopods seem to be missing – the ability to discern color. Instead, scientists believe that they detect intensities rather than colors. Cuttlefish are known to possess a single visual pigment with a peak sensitivity at wavelength 492 nm. When placed against a checkerboard pattern of blue and yellow squares that have the same intensity, cuttlefish cannot differentiate between the two colors and subsequently take on a uniform grey color.

Cephalopod colorblindness seems to present a baffling paradox and begs the question of how squids, octopuses, and cuttlefish can so expertly blend into their surroundings when they cannot detect basic colors. The answer may simply be that cephalopods don’t need the ability to differentiate between bright colors in a natural environment dominated by neutral tones. The reflectance spectra of cuttlefish chromatophores, which encompass yellow, orange, and dark brown hues, greatly overlap with the reflectance spectra of the substrates found in the cuttlefish’s natural surroundings. Furthermore, the variations in substrate and cuttlefish skin coloration are similar. This suggests that cuttlefish chromatophores evolved to match the colors found in natural habitats. With this appropriate color palate, intensity matching may be adequate for camouflage – especially in deeper waters with overall narrower wave bands of light. Furthermore, the cephalopod’s uncanny ability to match patterns and textures may be sufficient to fool predators.

The astounding accuracy and multi-dimensionality of cephalopod camouflage make it difficult to accept explanations of shortcuts, such as the ones described above to explain colorblind camouflage. However, cephalopod expert Roger Hanlon, who has studied over twenty cephalopod species over several decades both in the field and the laboratory, has recently proposed an ultimate shortcut; he believes that cephalopods employ just three basic templates to generate all of their coloration schemes. Hanlon has created three categories to explain all cephalopod camouflage patterns: uniform, mottled, and disruptive.

Uniform coloration is characterized by minimal variation in contrast. Mottled coloration employs repeated patterns of small light and dark patches. Lastly, disruptive coloration features patches that vary dramatically in color, shapes, scale, orientation, and contrast. Uniform and mottled camouflage allow cephalopods to match their backgrounds. The function of disruptive camouflage is to obscure the cephalopod’s true edge and to generate large conspicuous shapes that attract attention away from a recognizable outline.

Hanlon believes that cephalopods rapidly process visual cues and respond accordingly by choosing from among these three templates. For example, he has observed that the presence of white shapes against a dark background always triggers disruptive coloration in cuttlefish. Even more controversially, Hanlon believes that these three basic blueprints may govern all animal coloration patterns and adequately bamboozle predators across the animal kingdom.

Cuttlefish demonstrating uniform, mottled, and disruptive body patterns (from left to right) in response to different sized particles (sand, gravel, pebbles) and checkerboard backgrounds. (Roger Hanlon, MBL)

Investigating cephalopod camouflage can yield insight into the general patterns that govern camouflage for all animals. The cryptic coloration capabilities of modern cephalopods are unrivaled across all organisms. Scientists can further test Hanlon’s loaded conclusion that three patterns may govern cryptic coloration of all animals both by designing more manipulated experiments for cephalopods in the laboratory and by expanding their observations of cephalopods in the natural environment. Furthermore, the study of cephalopod camouflage can allow for a better understanding of cephalopods and the organisms that they interact with. For instance, by observing when cephalopods camouflage and the degree to which they do so, we can learn about the hunting schedule and visual capacity of cephalopod predators.

Because their neurological capacities are of interest to many scientists, cephalopods are among the most widely studied organisms. Yet countless aspects of the cephalopod’s striking ability to transform almost instantaneously into another creature or a constituent of its surroundings are still poorly understood. Dynamic mimicry, night-time camouflage, and colorblind camouflage all represent fascinating aspects of cephalopod camouflage that indicate natural selection patterns; however, evolutionary processes are often based on speculation rather than evidence. This evidence is likely to remain elusive unless we can fill in gaps from the fossil record.

This squid is double signaling - presenting white coloration to a female squid with one side of his body while displaying a zebra pattern to ward off other males with his other half. (Image by James Wood)

Furthermore, while we can infer that cephalopod camouflage arose initially from the need to avoid predators and to efficiently hunt prey, cephalopod uses for cryptic coloration have proliferated to include complex behaviors such as mating, communicating among conspecifics, and gaining a competitive advantage over rivals. One intriguing usage of cryptic coloration has been observed in squid that can “double signal” two messages simultaneously. Some male squids, for example, will manipulate half of their body to court with a female squid, while assuming a zebra pattern on the other half of their body to signal aggression towards other males. As the squid rotates or changes his position, he will instantaneously adjust his coloration patterns so that the zebra pattern is always on the side opposite the female. Thus, cephalopod camouflage is constantly developing and expanding into new behavioral adaptations.

Ultimately, modern cephalopods are a dynamic group of animals, from which we still have much to discover. They are unapologetically shrewd, endlessly amusing, and ever evolving. Their capacity to camouflage serves as a reminder of how staggering nature can be. Given their millions of pigment-containing cells, it’s no wonder that it’s never a dull moment with cephalopods.

For more reading on the evolution of cephalopod camouflage and intelligence:

Arnold, John, William Adelman, and Daniel Gilbert. Squid as experimental animals: Evolution and intelligence of cephalopods. New York, NY: Plenum Press, 1990. 3-7. Print.

Barbosa, A., Mathger, L.M., Buresch, K.C., Kelly, J., Chubb, C., Chiao, C.C., Halon, R.T. (2008). Cuttlefish camouflage: The effects of substrate contrast and size in evoking uniform, mottle, or disruptive body patterns. Vis. Res. 48, 1242-53.

Carlini, D.B., Reece, K.S., Graves, J.E. (2000). Actin gene family evolution and the phylogeny of colloid cephalopods. Mol Biol Evol 17, 1353-1370.

Chiao, C-C., and Hanlon, R.T. (2001). Cuttlefish camouflage: Visual perception of size, contrast, and number of white squares on artificial checkerboard substrata initiates disruptive coloration. Journal of Experimental Biology 204, 2119-2125.

Cloney, R.A. and Brocco, S.L. (1983). Chromatophore organs, reflector cells, iridocytes, and leucophores in cephalopods. Amer. Zool. 23, 581-92.

Fiorito, G. and Scotto, P. (1992). Observation learning in Octopus vulgaris. Science 256, 545-47.

Foote, M. and Sepkoski, J.J. (1999). Absolute measures of the completeness of the fossil record. Nature 398, 415-17.

Hanlon, R.T. (2007). Cephalopod dynamic camouflage. Current Biology 170, 1-5.

Hanlon, R.T., Conroy, L., Forsythe, J.W. (2007). Mimicry and foraging behavior of two tropical sand-flat octopus species off North Sulawesi, Indonesia. Biological Journal of the Linnean Society 93, 23-28.

Hanlon, R.T., Naud, M.J., Forsythe, J.W., Hall, K., Watson, A.C., and Mckechnie, J. (2007). Adaptable night camouflage by cuttflefish. Am. Nat. 169, 543-51.

Hanlon, R.T., Chiao, C-C., Mathger, L.M., Barbosa, A., Buresch K.C., and Chubb, C. (2009). Cephalopod dynamic camouflage: bridging the continuum between background matching and disruptive coloration. Philos Trans R Soc Lond B Biol Sci. 364, 429-37.

Hanlon, R.T., Watson, A.C., and Barbosa, A. (2010). A “mimic octopus” in the Atlantic: flatfish mimicry and camouflage by Macrotritopus defilippi. Biol. Bull. 218, 15-24.

Hewitt, R.A., Yoshilke, T., and Westermann, G.E.G. (1990). Shell microstructure and ecology of the Cretaceous colloid cephalopod Naefia from the Santonian of Japan. Cretaceous Research 12, 47-54.

Jaaro, H. and Fainzilber, M. (2006). Building complex brains – missing pieces in an evolutionary puzzle. Brain Behav Evol. 68, 191-95.

Kelman, E.J., Baddeley, R.J., Shohet, A.J., Osorio, D. (2007). Perception of visual texture and the expression of disruptive camouflage by the cuttlefish (Sepia officials). Proc. R. Soc. B 274,1369-75.

Mather, J.A. (2009). ‘Home’ choice and modification by juvenile Octopus vulgaris: specialized intelligence and tool use?. Journal of Zoology 233, 359-68.

Mathger, L.M., Barbosa, A., Miner, S., and Hanlon, R.T. (2006). Color blindness and contrast perception in cuttlefish (Sepia officinalis). Vis. Res. 46, 1746-53.

Mathgar, L.M. and Denton, E.J. (2001). Reflective properties or iridophores and fluorescent ‘eyespots’ in the loliginid squid Alloteuthis subulata and Loligo vulgaris. J Exp Biol 204 2103-18.

Mathger, L.M., Denton, E.J., Marshall, N.J., and Hanlon, R.T. (2009). Mechanisms and behavioural functions of structural coloration in cephalopods. J.R. Soc. Interface 6, S149-S163.

Mathgar, L.M., and Hanlon, R.T. (2007). Malleable skin coloration in cephalopods: selective reflectance, transmission and absorbance of light by chromatophores and irodophores. Cell Tissue Res. 329, 179-86.

Mathger, L.M., Shashar, N. and Hanlon, R.T. (2009). Do cephalopods communicate using polarized light reflections from their skin?. Journal of Experimental Biology 212: 2133-2140. (Featured Commentary)

Messenger, J.B. (2001). Cephalopod chromatophores: neurobiology and natural history. Biol. Rev. 76, 473-528.

Norman, M.D., Finn, J., and Tregenza, T. (1999). Female impersonation as an alliterative reproductive strategy in giant cuttlefish. Proc Biol Sci. 266, 1347-49.

Norman, M.D., Finn, J. and Tregenza, T. (2001). Dynamic mimicry in an Indo-Malayan octopus. Proc. R. Soc. Lond. B 268, 1755-58.

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