Nature’s best camouflage

Octopus camouflage. © Brandon Cole.

The masters of camouflage on this planet are universally accepted to be cephalopods, which can create optical illusions in the blink of an eye. An octopus or cuttlefish on a coral reef can produce effective camouflage on any of the hundreds of backgrounds that it encounters in this most complex of nature’s habitats. The selective pressure for this unique capability emanates from the extraordinary variety of visual systems of multiple predators, particularly fishes, diving birds, and marine mammals.

Camouflage is all about visual perception. Primarily it centres around the visual capabilities of various predators, but in the case of cephalopods it is also about their own visual capabilities and decisions about which camouflage tactic to deploy. Thus, having the ability to change camouflage brings with it the burden of developing a method to swiftly analyze a visual scene, extract its key features, and then deploy an effective camouflage pattern. This is a remarkable cognitive process that involves decision-making at a high degree. It begs three basic questions: what are the fundamental tactics of camouflage that deceive such a wide range of predators? How many camouflage patterns does an individual cuttlefish or octopus have the ability to produce? How quickly can they change their camouflage?

DYNAMIC CHANGES TO AVOID DETECTION OR RECOGNITION

Octopus cyanea on Pacific coral reefs change their appearance more than 150 times per hour while foraging each day! Fast change is needed because cephalopods are mobile and move into different visual scenes constantly when foraging. During their stop-and-go foraging trek, they change their camouflage pattern each time they stop and it is tailored to that particular background. The speed of change is remarkable. By studying video of naturally foraging octopuses and cuttlefishes, it is known that they change in a fraction of a second. That is, they can create patterns in their skin in as little as 200 milliseconds; complex patterns may take up to 2,000 milliseconds (2 seconds) but usually it is in the order of 200–300 milliseconds, which is the speed of a human eyeblink.

Camouflage is something that cephalopods do almost all of the time because they are soft bodied and their primary defence is to not be detected or recognised in the first place. This presents different challenges when they are swimming in the water column or down near the bottom, where there can be a great deal of structure and colour, or there can be open sand or mud plains that create different survival challenges.

The fundamental tactics are: 1) remain undetected; 2) disrupt body form so that the cephalopod is not recognisable as a distinctive octopus, cuttlefish, or squid; or 3) look like an uninteresting or distasteful object. Most animals in other phyla use one of these tricks, but cephalopods use all three with variations on each for unparalleled diversity.

Disruptive patterning is a less obvious way to attain camouflage. Some disruptive patterns of cuttlefishes tend to blend into the background while other disruptive patterns—even shown by the same animal—are clearly detectable yet they render the cuttlefishes very difficult to recognise because they create false edges and put on light and dark patches of variable size, shape, and orientation so that it is hard to distinguish head from mantle, front from back.

Octopuses are very adept at background matching. However, due to their very flexible arms and non-rigid body mantle, they can contort themselves to cause visual disruption without creating as many skin patches as are needed by cuttlefishes or squids.

MIMICRY & MASQUERADE

Juvenile cuttlefish camouflaged against the seafloor.

Mimicry is looking like another animal, while masquerade is looking like an uninteresting object. Both tactics confuse recognition, and both can be found in certain cephalopods. Mimicry is commonly understood to imply the resemblance of one animal (the mimic) to another animal (the model) such that a third animal (a predator) is deceived by their physical similarity into confusing the two. Only three cases of defensive mimicry are authenticated in cephalopods and all three are octopuses. The so-called “mimic octopus” and the undescribed “white V octopus” of tropical Indonesia, and the Caribbean long-arm octopus Macrotritopus defilippi mimic the shape, colouration, and swimming speed of local flatfish when they are moving. All three species live in open sandy flats where they would be detected by predators, so the guise is to look like some other animal.

Masquerade is widespread among shallow-water octopuses, cuttlefishes, and squids. To a human observer, cephalopods can sometimes look like stones, algae, seagrasses, and other objects such as soft and hard corals. Octopuses, cuttlefishes, and squids all use arm postures to enhance masquerade matching, and they are very good at using their vision to decide when and how to position their arms to help match nearby objects.

MOTION CAMOUFLAGE

Motion camouflage is moving in a fashion that decreases the probability of detection by a predator. Octopuses are good at this—they can move with stealth across open areas without being recognised. The cognitive aspects of this behaviour are noteworthy because the speed of the octopus is generally similar to the speed of rippling light in that environment, suggesting that the octopus consciously regulates its stealth speed in accordance with ambient motion such as dappled sunlight from waves. Moreover, they can change their overall body shape and skin texture according to other three-dimensional objects in the distant background as shown in the illustration below, based on Octopus vulgaris in the Caribbean. That is, they can perform the “moving algae” trick when spiky algae are nearby, or the “moving rock” trick when smooth coral heads or rocks are nearby.

WHEN CAMOUFLAGE FAILS

Warning display of greater blue-ringed octopus. © Jens Petersen.

When the primary defence of camouflage fails, as it sometimes does, cephalopods have a two-stage response of secondary defences that startle then confuse predators.

The first stage—termed deimatic behaviour—is meant to make the predator hesitate in its attack sequence. The second stage—termed protean behaviour—involves complexes of erratic unpredictable escape manoeuvres, colour changes, and behaviours. Together, these constitute a formidable defence strategy suitable for the soft-bodied cephalopods, which are otherwise quite defenceless.

MULTIPLE ESCAPE TRICKS

To interrupt the first stage of attack, cephalopods first use either a Stay or a Go tactic. The “Stay” tactic is a conspicuous deimatic display in which an octopus spreads the web between its arms to look bigger than it is and makes a large dark spot around the eyes to startle the prey to make it hesitate just temporarily. Conversely, they may immediately ink and jet away, which is a “Go” tactic.

This is immediately followed by erratic unpredictable escape manoeuvres. This phase of secondary defence is aptly called protean behaviour after Proteus—the Greek god of unpredictability. These behaviours can be very complex—some octopuses can mix signals, manoeuvres, and camouflage up to ten times in just 13 seconds.

TAILORED ESCAPE TO DIFFERENT PREDATORS

In filmed sequences underwater, as well as during laboratory experiments, it was found that cuttlefishes are capable of recognizing different predators and they modified their secondary defenses accordingly. This was true even for hatchling cuttlefishes that had no experiences with predators, so this initial recognition represents an innate ability. Thereafter, however, the cuttlefishes were continually making decisions about how to implement protean behavior and they did so according to the microhabitat they were in at the time. This sort of swift sensory processing and decision-making is characteristic of high-level cognitive processing that large brains can enable.

Dr Roger Hanlon PhD is the Senior Scientist at the Marine Biological Laboratory in Woods Hole Massachussetts and Professor of Ecology and Evolutionary Biology at Brown University. His book Octopus, Squid & Cuttlefish: The worldwide illustrated guide to cephalopods is available now: https://amzn.to/2O0B6lK