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Authors: Roland C. Anderson

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During that summer, Olive behaved normally for a giant Pacific octopus guarding eggs: she refused food, she was never seen out of her den, she constantly kept the eggs clean, she repelled predators and egg eaters, and she grew unresponsive to divers, maintaining a gray color that gradually turned to a translucent white. Her eggs were white when first laid, but gradually changed to a yellow color as the embryos grew within, and then turned brown with chromatophores just before hatching. Divers saw eyespots inside the eggs in mid June, about 110 days after the eggs were laid, so they knew the eggs were fertile.

Divers witnessed the first of Olive's eggs hatching on a night dive on September 22, 209 days after the eggs were laid. While a few of the paralarvae swam out of the den during the daytime, Olive blew most of them out of the den at night. She may have been causing them to hatch at night by blowing
strong water jets over them. At this point, she was totally white, almost translucent. Her skin had several large white ulcers on her arms and mantle, and it had the appearance of rotting away. She was totally unresponsive to divers, even when touched, devoting her remaining energy to her eggs.

The peak of the paralarval hatching was October 7, 224 days after she laid her eggs. Divers saw the last hatchlings on October 31, and at that time there were virtually no eggs left unhatched. Olive was dead on November 6, 254 days after laying her first eggs. Her body was about 6 ft. (2 m) from the opening of her den, being fed on by two sea stars. Nothing goes to waste in the sea, and scavengers are always waiting for the chance to clean up dead bodies.

The precise timing of her death to the last hatching of her eggs is remarkable. Although it sounds anthropocentric, it looked as though she clung to life until she knew her eggs hatched. It is also remarkable that she was able to bring her eggs to successful hatching considering her circumstances. Her den was located within Seattle's inner harbor, next to the outlet of a river that flows through an industrial area. The river and the harbor were once very polluted. Her success may be a testament to our modern pollution clean up efforts and awareness of the necessity of keeping pollutants out of rivers and bays, or it may simply reflect the durability of this female and her eggs.

Olive was visited almost daily by curious divers. Her home was Washington state's most popular dive site, used by many dive classes as their first open-water dive each week, since the location is sheltered from storms and their waves. Her success despite all these disturbances is also a testimonial to her dedication to the eggs.

The saga of Olive the Octopus brooding her eggs in Seattle's harbor was covered by several local newspapers and magazines. The reading public was entranced with her story and saddened by her death. The diving community also mourned her death. One dive magazine ran an article about her, “So Long, Olive, We Barely Knew You,” lamenting the short life span of octopuses.

Many octopus eggs take a long time to develop. While the 224 days Olive's eggs took to hatch is a bit more than the about six months reported for the species, this egg development period is by no means the longest for an octopus species. Egg development time is dependent on the temperature of the water: the colder the water, the longer the development period within the egg. Eggs of the giant Pacific octopus in California have a four-month
development, while those in Seattle or Alaska may take seven to eight months to hatch. The spoon-arm octopus of the North Atlantic and the Arctic Ocean lives on the continental slope, in water that is 600 to 1200 ft. (200 to 400 m) deep and a temperature of about 35°F (2°C). James has raised this type of little octopus through several generations, and he has found that their eggs take over a year to hatch out into benthic juveniles, ready to take up the bottom-dwelling existence of their parents.

Most deep-water octopuses have large eggs with long development periods that hatch out looking like their parents. This is logical when you consider where they live. There is nothing small like plankton in the ocean depths for the paralarvae to eat, so they must be large enough to be able to eat larger organisms. Some moderately deep-water fish spawn eggs that float to the surface waters, where their hatchlings live in the plankton, only to swim deeper when they are older and large enough to undertake such a vertical migration. But they may only migrate down a thousand feet or so. Other deeper-living fish and octopuses don't use this risky strategy, nor do most other creatures that live a mile deep.

Biologists Janet Voight and Tony Grehan, filming a rocky outcrop rising above the muddy abyssal plain off the west coast of Canada from a submersible in 2000, made a fascinating discovery: they saw twenty-eight female octopuses (of unknown deep-water species) guarding eggs laid on the rocks. They had laid eggs in different places and each had laid fewer than 100 large eggs, attached singly to the rocks. Some of these eggs were the largest known of any octopus, about 2 in. (5 cm) long. After some of these eggs were collected, they hatched out into the largest octopus hatchlings known to science. One female was still guarding her eggs in the same location a year later, and she looked senescent the second year, much like Olive toward the end of her brooding period. Based on the rate of development of the eggs, their size, and the temperature of the water at those depths, we believe it may take up to four years for the eggs of this species to hatch, presumably guarded all the time by a fasting female octopus. At least the deep-water females don't have as many predators to watch for as the shallow-water species do, but the brood time is remarkable. The possibility that the female doesn't eat during such a long guarding period is something to think about, and extrapolation from the brooding time leads to a possible life span of that species of over ten years, the longest for any octopus. Everything's slower in the deep.

Researchers have collected developing octopus eggs and viewed them
under light with low-power microscopes or opened them up to see several stages of the development that occurs inside the egg. Huge changes take place in the egg capsule, starting with a cell and ending up with a complete and fairly well-developed animal. Since the egg capsules are usually opaque, embryologists (who study development before birth) can sometimes see what's going on inside, but often they have to open up an egg, preserve the embryo, and study it later. The single fertilized egg cell divides into clumps of cells, arranged in blastula and then gastrula stages. Gradually these cell collections begin to specialize, and we can see the beginning of the adult organs. Meanwhile, the little embryo flips its position in the egg twice, ending up with its mantle pressed against the opposite end from the attachment, ready to push out in the world during hatching.

When does an egg become an octopus? The changes are gradual; there's no specific time, as in all embryological development. First, the yolk develops to nourish the embryo and can be seen extending toward the egg capsule attachment. Then the arms develop, first visible as eight arm buds around the yolk and gradually getting longer (though the planktonic octopuses like the giant Pacific octopus don't have very long arms at birth). The eyes begin to develop at this point, and since they are dark with their pigment, anxious aquarists and the divers visiting Olive could see them through the capsule and know the eggs had been fertilized. Next, the heart begins to develop well enough to be an organ and to beat. The final part of the octopus that can be seen to develop is the chromatophores—there are not many of them and they are conspicuously large in the semitransparent skin. All through the embryonic period, the yolk is used to nourish the embryo, and by the time of hatching, none is left. Sometimes an octopus is disturbed during her brooding, and she may inadvertently push the eggs around so they hatch early. If so, they will have remains of the yolk sac like a deflated balloon sticking out from between their arms.

Hatching must be a traumatic event in the life of the octopus embryo, just as being born is to humans. We go from being cushioned, warmed, protected, and nourished by our mothers inside their bodies to living by ourselves. We go from not having to breathe to having to expel liquid from our lungs and drawing our first breath. Through the course of vigorous muscular contractions, we are expelled out the birth canal into the external world, much like other mammal babies. Chickens and other birds have to chip their way out of their tough eggs. Frequently the chicks have a hatching tooth that helps them penetrate the eggshell, which is later resorbed
or falls off as the chick grows up. Some reptile mothers such as crocodiles help the eggs hatch by gently cracking the eggs, and mother octopuses may also help the eggs hatch.

Octopus hatching occurs with the aid of a hatching gland, a collection of enzyme-containing cells on the mantle of the embryo that help dissolve the chorion (egg shell), along with violent expansions and contractions of the mantle. The little octopus paralarva breaks mantle-first through the distal end of the egg, popping out in the normal swimming posture of a jetting octopus. The octopus lives on a remnant of its yolk sac for the first few days, but that is soon absorbed, and the hatchling must find food for itself. Benthic hatchlings, like those of the Caribbean reef or Californian two-spot octopus, just crawl away, but paralarvae of species such as the red octopus take up the life style of a drifter, swimming in the rich surface waters of the sea.

2

Drifting and Settling

W
hile most octopuses live on the sea bottom, the situation is different for the newly hatched young. The many species of octopuses have two different life style strategies as hatchlings. These differences come from the size of the eggs, not the size of the adult animals: the giant Pacific octopus is one of the biggest octopuses but has tiny young. Most octopus species lay small eggs that produce small baby octopuses that are planktonic—they get washed away by ocean currents and temporarily live in the plankton-rich surface waters of the ocean. A few species lay large eggs that produce benthic hatchlings, big enough to live on or near the bottom of the ocean.

Living in the plankton requires adaptations, especially for the early stages of an animal like the octopus that later spends its adult life crawling on the bottom of the ocean among the rocks or coral. To understand why many young octopuses start their lives in the plankton, we must understand what plankton is, how the plants and animals that comprise plankton live, what methods they use to keep from sinking, what they eat, how they swim, what preys on them, and how they avoid being eaten. We must understand the advantages and disadvantages of living in the plankton, the bigger ecological implications of having a life stage different from that of an adult, and the adaptations and changes needed to live that life stage in that environment.

The word “plankton” is derived from the Greek root word that means free floating or wandering. The term is applied to any plant or animal that is unattached and floating in the surface waters of the ocean as well as to any weak, swimming animal that cannot swim against the ocean's currents. Even some comparatively large creatures such as jellyfish and the open-ocean argonaut octopus are part of the plankton. Relatively huge creatures such as sea turtles and ocean sunfish, which are weak swimmers, are sometimes considered planktonic. Plankton includes marine bacteria,
animals, and plants, and some swimming animals that have plant pigments that undergo photosynthesis (making food from carbon and oxygen), which is normally a plant trait.

In her poem Plankton, Joan Swift wrote:

They live their lives unseen

Not just gray mobs without faces

But like calm, steady workers

In some underground plot

To keep the world alive.

Plankton does indeed keep the world alive and is pretty much unseen and under-appreciated.

Animals and plants living in the plankton are the most important organisms in the ocean, but they are neither the most visible, the best known, the most highly beloved, nor the most feared. They are not the whales, the sharks, or the sea stars. They are not the familiar animals we eat, such as clams or oysters. They are not the organisms we mostly study, like porpoises, or the animals we capture to exhibit in public aquariums. They are usually not octopuses, although some octopuses are part of plankton as juveniles and a few as adults. In The Log from the Sea of Cortez (1951), writer John Steinbeck said that the disappearance of plankton, although the components are microscopic, would in a short time probably eliminate every living thing in the sea and ultimately the whole of human life. Since he wrote that, we have learned of the ecological communities surrounding the deep-sea hydrothermal vents that are not dependent on plankton for their survival, but instead depend on the hydrogen sulfide there, and they use bacteria to break it down and gain energy. But everything else in the ocean depends on plankton.

Plankton can be divided into plants (phytoplankton) and animals (zooplankton). Most animal phyla have representatives in the plankton, at least at some stage of their lives, since many animals such as fish and octopuses spend their juvenile stages there. Those creatures that are only in plankton temporarily are known as meroplankton, such as octopus paralarvae, while those that spend their whole lives there are called holoplankton, such as small single-celled plants, or diatoms.

The animals and plants of the plankton are extremely important to the ecology of the oceans. First, the plankton provides food for most of the ocean's other animals. Phytoplankton provide food for zooplankton, which in turn are eaten by fish and by other tiny organisms like paralarval octopuses. Little fish are eaten by big fish, and fish are eaten by sea birds, squid, marine mammals, and humans. The world's largest fish, the whale shark, and the world's largest animal, the blue whale, both live on plankton. Dead plankton and their waste products drift down to provide food for mid-water animals and those living on the abyssal bottom. The numbers of animals and plants in the plankton are tremendous. Terrestrial insects represent the most species (over a million have been described), but there are more copepods, small weak-swimming crustaceans, in the ocean than any other animal on earth.

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