One dedicated deep-sea octopus is now the world record holder for the most outlandishly long egg development. A female Graneledone boreopacifica off the California coast was observed guarding her eggs continuously for nearly four and a half years.
This eclipses the previous record holder for prenatal guardianship, the alpine salamander, which keeps its offspring internally for up to four years. Most animals that lay eggs watch them for a much shorter period of time. The record-holding fish, the Magellan plunderfish (Harpagifer bispinis), stays over its eggs for four to five months. And before these new observations about the California cephalopod, the longest confirmed octopus egg guarding was 14 months—a female Bathypolypus arcticus observed in a lab. "We were sure surprised," says Bruce Robison, a senior biologist at the Monterey Bay Aquarium Research Institute and co-author of the report, which was published July 30 in PLoS ONE. "The results we measured substantially exceeded everyone's expectations.”
"This far exceeds my expectations—which were long," says Janet Voight, an associate curator at The Field Museum in Chicago, who has been studying deep-sea octopuses for decades.
Octopuses are not generally long-brooding animals Most shallow-water octopods emerge in less than a few months, possibly because after laying her eggs a female octopus is on watch 24/7, tending and cleaning the eggs until they hatch.
"She'll be there, man"
In April 2007 Robison and his colleagues were conducting a regular survey of the Monterey Canyon off the central California coast, poking along 1,397 meters below sea level with a remotely operated vehicle (ROV), and found a lone G. boreopacifica octopus. They spotted this same female, which had distinctive scars, again on the next dive in May. This time, she had a brood of eggs.
The group returned 18 times during the next four and a half years to find the same octopus, in the same location, guarding the same clutch of eggs. Because nearly all octopuses lay just a single batch of eggs in their lifetimes and because the researchers tracked the eggs’ growth with laser measurements, the team was convinced that they were watching the very slow development of just one group of eggs. It was only after 40 months, for example, that the researchers could see the shape of the growing octopuses inside the eggs.

Each time the team sent the ROV down from their ship to conduct the survey, "scientists and pilots would speculate on whether she would still be there or not," Robison recalls. "As the months piled up the scientists grew more skeptical. The pilots, on the other hand, had more faith, [saying], 'she'll be there, man.'" 
Wasting away
During the long brooding period the female, who once had textured, purple skin, turned a pale white, losing muscle tone and developing cloudy eyes—signs of senescence, the rapid aging that precedes natural octopus death.
Throughout the many dives, however, Robison and his team never saw the female leave her eggs. "It is readily possibly that the female would not eat," Voight says. The animal may have stayed alive with a very slow metabolism, thanks to cold water and inactivity. Once, the researchers even tried to offer the octopus a piece of crab to see if she would eat it. She would not. "Eventually, as she became emaciated and frail-looking, even the ship's crew would crowd into the control room to see if she was still hanging in there," Robison says.
The last time the team saw the G. boreopacifica female was in September 2011. The next month there were only tattered remnants of the egg casings, evidence of a successful hatching. "On the final dive, when we found her gone, the common reaction was relief that her ordeal was over, tinged with regret that we wouldn't see her again," Robison recounts.
A different strategy
In contrast to shallow-water octopuses, which often lay thousands of tiny eggs that hatch into planktonlike paralarvae, this female seemed to have just 160 or so large eggs, which grew to about 3.3 centimeters. G. boreopacifica octopi emerge the most highly developed of any known octopus species, Voight described in a paper a decade ago.
The reproductive strategy, despite its differences from most other octopuses, "appears to be working, given the species's success," Robison says. As deep-sea octopuses go, this species is a relatively common sight on ROV dives into far-down trenches.
This long brooding process also suggests a relatively long life span for this species, a rarity when most octopuses live only a year or two. "The observations [here] provide an excellent benchmark for understanding longevity and brooding history," says Eric Hochberg, curator emeritus at the Santa Barbara Museum of Natural History. Hochberg has observed unknown species of Graneledone brooding "egg balls" of 80 or so very large eggs among their arms. Given the size of those eggs and cool water temperatures, he suggests these and other species might well also brood their eggs for more than four years.
And their reproductive histories may hold further surprises. "There is still much to learn about the life history of deep sea cephalopods," he says.