Researchers at the University of Rhode Island and the Monterey Bay Aquarium Research Institute have observed a deep-sea octopus brooding its eggs for four-and-a-half years -- longer than any other known animal. Throughout this time, the female kept the eggs clean and guarded them from predators. This feat represents an evolutionary balancing act between the benefits to the young octopuses of having plenty of time to develop within their eggs, and their mother's ability to survive for years with little or no food.

"This research demonstrates how little we know about life in the deep-sea and life generally," said Brad Seibel, a URI associate professor of biological sciences. "From shallow-living species we have developed limited and limiting ideas about the capabilities of animals."

Based on previous research, Seibel had postulated that eggs of some deep-sea octopus could take years to develop, and this new observation provided a perfect opportunity to test that hypothesis. "While we predicted a long development time, our confidence in that prediction was not high and our result was still surprising."

Every few months for the last 25 years, a team of Monterey Bay researchers led by Bruce Robison has performed surveys of deep-sea animals at a research site in the depths of Monterey Canyon that they call Midwater 1.

In May 2007, during one of these surveys, the researchers discovered a female octopus clinging to a rocky ledge just above the floor of the canyon, about 4,600 feet below the ocean surface. The octopus, a species known as Graneledone boreopacifica, had not been in this location during their previous dive at this site in April.

Over the next four-and-a-half years, the researchers dove at this same site 18 times. Each time, they found the same octopus, which they could identify by her distinctive scars, in the same place. As the years passed, her translucent eggs grew larger and the researchers could see young octopuses developing inside. Over the same period, the female gradually lost weight and her skin became loose and pale.

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The researchers never saw the female leave her eggs or eat anything. She did not even show interest in small crabs and shrimp that crawled or swam by, as long as they did not bother her eggs.

The last time the researchers saw the brooding octopus was in September 2011. When they returned one month later, they found that the female was gone. As the researchers wrote in a paper published this week in the journal PLOS ONE, "the rock face she had occupied held the tattered remnants of empty egg capsules." After counting the remnants of the egg capsules, the researchers estimated that the female octopus had been brooding about 160 eggs.

Most female octopuses lay only one set of eggs and die about the time that their eggs hatch. The eggs of Graneledone boreopacifica are tear-drop-shaped capsules the size of small olives. As the young develop inside the eggs, they require plenty of oxygen. This means that the female octopus must continuously bathe the eggs in fresh, oxygenated seawater and keep them from being covered with silt or debris. The female must also guard her eggs vigilantly to prevent them from being eaten by predators.

Because the young octopus spend so much time in their eggs, by the time they hatch they are fully capable of surviving on their own and hunting for small prey. In fact, the newborns of G. boreopacifica are larger and better developed than the hatchlings of any other octopus or squid.

Long brooding times present an evolutionary challenge, especially for animals such as octopus, which do not live very long. As the authors noted in their paper, "The trade-off within the reproductive strategy of deep-living octopods is between the mother's ability to endure a long brooding period and the competitiveness of her hatchlings. Graneledone boreopacifica produces hatchlings that are very highly developed, which gives them the advantage of a high potential for survival."

This research suggests that, in addition to setting records for the longest brooding time of any animal, Graneledone boreopacifica may be one of the longest lived cephalopods (a group that includes octopuses, squids, and their relatives). Most shallow-water octopuses and squids live just a year or two.

"The ultimate fate of a brooding female octopus is inevitably death," the researchers wrote, "but in this first example from the deep sea, brooding also confers an extension of adult life that greatly exceeds most projections of cephalopod longevity."