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Authors: Roland C. Anderson

BOOK: Octopus
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When a potential predator gets too close to an occupied octopus's den, the octopus may deter the predator by jetting a blast of water at it from its funnel. Octopuses mostly use this method to get rid of annoyances, such as nonthreatening fish like perch or rockfish in the northern Pacific, or parrotfish and wrasse in tropical waters. Humans trying to sample shells from the midden can also annoy octopuses and receive a water blast. When researchers were extracting giant Pacific octopuses from their dens for scientific study by squirting a noxious chemical into the dens, often the chemical was blown right back out at the researchers by the octopuses' water jets.

Octopuses jetting water at annoyances can lead to some amusing consequences. In the late 1950s, a researcher named Peter Dews wanted to conduct a standard learning experiment with an octopus, so he set up a
situation in which three common octopuses had to pull a lever to get food. Two octopuses learned the process easily, but the third, named Charles, was a challenge. In Dews's words, “Charles had a high tendency to direct jets of water out of the tank; specifically they were in the direction of the experimenter.” This octopus was either annoyed by the researcher or had a low tolerance for annoyances in general. Individual octopuses have different personalities, and octopuses with some temperaments just aren't suitable for this kind of experimentation. Charles eventually pulled the lever out of the tank wall.

At the Seattle Aquarium, there was a female octopus with an aggressive personality. This octopus would squirt water out of her tank at a particular employee, a night staffer, sending a large amount of water directly at the person each time she checked her during the night. The night staffer got soaked from this unexpected midnight shower, and became irate when she thought the octopus was singling her out for special humiliation. We eventually figured out that the staffer was shining her bright flashlight on the octopus tank to check the water inflow and outflow. The octopus rightly associated this midnight disturbance with the staffer and showed her annoyance by jetting at her.

We witnessed an amusing example of octopuses jetting at annoyances in Hawaii. We were observing a Hawaiian day octopus in an enclosed saltwater pond on Coconut Island. It sat on the edge of a concrete slab that had fallen to the bottom of the pond, just outside the den it had excavated under the slab. A butterfly winged erratically over the pond above the octopus. When it came close to the water surface, the octopus blew a sudden strong burst of water straight up through the 1-ft. (30-cm) depth of water. The water erupted like a geyser beneath the butterfly, which darted away quickly.

Since octopuses face many types of predators, they use a variety of means to avoid getting eaten while out of their dens looking for food or mates. Their first line of defense is not getting seen and therefore they use camouflage. The octopus species in shallow tropical waters may be the best color-change artists of the cephalopod world. They live on, work in, and camouflage to the multihued coral reefs. In northern waters, octopus species live in darker water frequently clouded with runoff sediments or plankton, and at those latitudes the sun is at a lower angle, so octopuses and fishes there specialize in grays, reds, and browns. Deeper in the ocean, along the continental shelf or into the abyssal plain, octopuses are almost
uniformly muddy brown or gray because there is no light there. Deep-sea predators may still possess eyes only to detect bioluminescence from other animals.

If camouflage doesn't work and a potential predator gets closer, an octopus may go to a different strategy, still using a change in appearance. It may use a bluff behavior: it either makes itself look bigger than it actually is, or it may assume the appearance of something else entirely, something that isn't a tasty octopus. This mimicry, or deimatic display, in cephalopods is an example of a display that startles a predator and makes it hesitate before attacking. The deimatic display is remarkably similar in many types of cephalopods. Cuttlefish show it by turning pale and putting on two dark spots near the posterior end of their mantle. Caribbean reef squid show it with a varied number of dots.

Shallow-water octopuses also produce eye patterns, showing two dark areas on the pale background of their skin around the eye while spreading the arm web wide and paling it, making them look much bigger than they are and mimicking an animal with big eyes set wide apart. Some species have permanent eyelike colored spots, or ocelli, in the skin in front of and below their real eyes, which they can intensify to make them look brighter. Although the ocelli may be used for deimatic display, observers can also use them for species identification.

The deimatic display is similar in several shallow-water cephalopods. Since these ocelli are located on different areas of the skin in different cephalopods, the display probably evolved in parallel, with different animals arriving at the same solution to the same problem, or convergent evolution. Animals in other phyla, such as the four-eyed butterfly fish and the luna moth, use a similar eyespot display.

There is some debate as to how octopuses use deimatic behavior and display. Deimatic display among squid is used in cases of mild threat, such as a big parrotfish getting too close to a squid. No effect has yet been established for the use of deimatic display in octopuses. Studying antipredator behavior among octopuses is a challenge because scientists rarely get to see predation events. We've witnessed lots of evasion behavior, but there hasn't been much chance to see it fail.

In addition to camouflage, octopuses use other defense behaviors while out of the den. Hanlon et al. (1999) observed that when predators approached, day octopuses changed their body patterns three times a minute when they sensed a threat, using patterns that were at times cryptic, conspicuous,
and even mimicking of fish. They speculated that such changeability in body patterning prevents predators from developing a search image for octopuses. One particularly fascinating behavior they saw was an octopus crawling across a sand flat from one coral reef to another. The octopus perfectly resembled either a coral rock or a ball of detached algae as it moved across the sand, tiptoeing on its suckers. It was conspicuous against the sand but camouflaged perfectly to resemble the growth on the coral rocks of the reef yards ahead of it.

If camouflage or startle behavior doesn't work in avoiding predators, an octopus has more evasion techniques at its disposal before it would have to fight for its life. If given the opportunity, it will try to flee rather than fight with a predator or larger octopus. Shallow-water octopuses have a fairly typical escape response when predators get too close. First they turn pale all over, eject a cloud of ink, and jet away. Then they settle onto a new spot and quickly camouflage to match it. An octopus may use only one of these actions, or, when under the most threat, it might do all of them in sequence.

The octopus's sequence of paling-inking-jetting-camouflage has a confounding effect on a potential predator. First, the octopus is gone or appears to have disappeared very quickly. In general, octopuses don't swim as well as squid, but they can swim quite fast over short distances using jet propulsion. They usually swim a relatively short distance, hopefully to a pile of rocks or coral, where they can crawl in and hide or quickly camouflage, or just out of a predator's sight.

Avoiding a predator by blowing a blob of ink in its direction can have several effects. Octopus ink is largely formed of melanin, one of the blackest, most opaque substances produced by animals. Cephalopod ink was used in ancient times as the first ink for writing, and sepia ink is named after the common cuttlefish, Sepia sp., that provided it. Ink was produced by the earliest of the octopuses' coleioid ancestors. The fossilized ink sac from a 65-million-year-old cuttlefish, when ground up and mixed with alcohol, still made very good writing ink.

Octopus ink can be different colors in different species. One way to distinguish between the two sibling species of two-spot octopuses in southern California is their ink: one produces black ink and one produces brown. Nocturnal species of octopuses and deep-water octopus species may produce a deep red ink. As seawater filters out red light, the red color
of this ink is absorbed quickly in water, so red ink looks the same as black in the deep.

The ink sac of an octopus sits underneath its digestive gland. It is composed of a small gland that actually produces the ink and a larger sac where it is stored. The sac has an extended duct that leads to the anus of the octopus and vents into the funnel. The ink duct itself has several pouches where ink is stored, ready for quick discharge out the funnel with a vigorous water jet.

Along the way to the octopus's funnel, the ink passes through glands, where it is mixed with varying amounts of mucus. The mucus gives differing consistencies to the vented ink. The funnel ejects the ink in a blob of a certain form. Some cephalopods eject ink in a blob about the same size and shape as their bodies, and so they leave a phantom squid or octopus (a pseudomorph) hanging in the water as they turn pale and jet away. Hawaiian bobtail squid leave a phantom squid blob several times in succession, each about 1 yd. (1 m) apart. Sometimes a squid then turns dark and hangs in the water at the end of the string of ink blobs, further confusing the predator by imitating the blobs. In lab tests, we saw that both the bobtail squid and the stubby squid (Rossia pacifica) could vary the consistency of their ink blobs from a diffuse cloud to a thick blob. In the Caribbean, we have seen squid ink blobs drifting in the current that came from a school of squid hundreds of yards upcurrent, proving the ability of an ink blob to hold its shape long after it is formed.

Octopus ink can also be squirted out in a long string as the octopus swims away. Most octopuses squirt the ink out in a big loose cloud, with little or no mucus mixed in. In this form, it has two functions. The first is to act as a smokescreen to hide the octopus from the predator's view while it camouflages against the bottom or turns transparent, jets away, and then camouflages again. Such ink clouds can be very large, many times the volume of the octopus that created them. Even a common octopus or a day octopus can make an ink cloud large enough to screen from divers, and a 75-lb. (34-kg) giant Pacific octopus can expel enough ink to obscure vision throughout a 3000 gallon (12,000 l) tank.

In addition to blocking a predator's sight, cephalopod ink contains tyrosinase, a highly irritating substance that temporarily paralyzes the sense of smell of a predator and also irritates its eyes. The mucus in the ink can also clog a fish predator's mouth and gills. Ink is such an effective defense
that almost all cephalopods possess ink sacs. There is fossil evidence that ancient ammonites, belemnites, and even some fossil nautiloids had them. All species in the genus Octopus have ink sacs. The modern cephalopods that don't have ink sacs probably lost them through evolution. Other groups of octopuses, mainly deep-water types such as the vent octopus, don't have ink; ink would be no use in the depths where there is no light to see. The velvet octopus (Grimpella thaumastocher), a shallow-water octopus, doesn't have ink. It may have evolved from deep-water species and then moved into shallow water. We tend to believe that deep-water octopus species evolved from shallow-water ones, but maybe not always.

Some octopuses and other cephalopods have adapted their use of ink. One species of deep-water squid, Heteroteuthis dispar, doesn't seem to have melanin in its ink but instead expels a bioluminescent cloud. Since it's not effective to use black ink in the dark depths, and these little creatures can't make light by themselves, they culture bioluminescent bacteria in their ink sacs for use when they want to make some light. It must be thoroughly astounding to see these squid responding to a threat by spewing out this light cloud in the depths.

Some open-ocean cephalopods are barely visible. The glass octopus normally has transparent body parts and is barely visible, giving us an idea of the invisibility of tiny octopus paralarvae. In the face of a threat such as an ROV, or submersible, with its bright lights, glass squid can turn themselves inside out, then blow their mantle cavity full of dark ink, and look like a black basketball floating in the dark water. Maybe they are presenting another form of camouflage and they just don't look like edible squid, or maybe a predator who tries to eat them ends up with a mouthful of noxious ink.

Another amazing use of ink can be found in the broadclub cuttlefish (Sepia latimanus). Cuttlefish are known for their ability to produce the Passing Cloud. Broadclub cuttlefish can move the dark pattern across their skin from the posterior to anterior of the animal. We have photographed a cuttlefish displaying a broad Passing Cloud from the posterior forward, culminating with a squirt of ink toward another cuttlefish. This passage of a dark blot on the animal to the water is another way to confuse a potential predator about where the animal actually is.

The mimic octopus displays other bizarre and enigmatic defensive behaviors. This species, which has only recently been described by taxonomists, lives in sand and muddy areas of shallow-water Indonesia. Its claim
to fame is its supposed ability to mimic the shape and behavior of other animals—animals that are less likely to get eaten than a tasty octopus. This octopus can flatten its body and move across the sand, using its jet for propulsion and trailing its arms, with the same undulating motion as a flounder or sole. It can swim above the mud with its striped arms outspread, looking like a venomous lionfish or jellyfish. It can narrow the width of its combined slender body and arms to look like a striped sea snake. And it may be able to carry out other mimicries we have yet to see. Particularly impressive about the mimic octopus is that not only can it take on the appearance of another animal but it can also assume the behavior of that animal.

The mimic octopus has become well known because of its defensive behaviors. Photographs of this octopus have been published and its behavior captured on film for television nature shows. Few people have seen or photographed the mimic octopus, because it lives in such a remote location and because few divers dive on the mud flats where it lives. Mimic octopuses have proven impossible to keep in captivity, even though they occasionally show up in pet stores. Roy Caldwell (2000) presents a good case for not buying these fascinating creatures: he believes that overfishing for the aquarium trade may drive the species toward extinction.

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