In April of 2007, Bruce Robison sent a submersible into a huge underwater canyon in California’s Monterey Bay. At the canyon’s base, 1400 metres below the surface, he spotted a lone female octopus—Graneledone boreopacifica—crawling towards a rocky slope.

The team sent the sub to the same site 38 days later and found the same female, easily recognisable through her distinctive scars. She had crawled up the slope itself and was guarding a group of 160 small, milky teardrops cemented to the rock. They were eggs.

For many a female octopus, laying eggs marks the beginning of the end. She needs to cover them and defend them against would-be predators. She needs to gently waft currents over them so they get a constant supply of fresh, oxygenated water. And she does this continuously, never leaving and never eating.

When the eggs hatch, she dies, starving and exhausted. As biologist Jim Cosgrove says, “No mother could give more”. You can watch a giant Pacific octopus going through this surprisingly moving sacrifice in the clip below from the BBC’s wonderful series Life.

Biologists rarely get a chance to measure how long these brooding periods last; at Monterey Bay, Robison’s team had a rare opportunity. For four and a half years, they returned to the same spot and found the same octopus, “clinging to the vertical rock face, arms curled, covering her eggs”.

She never left, and it’s possible that she didn’t eat for the whole time. Tasty crabs and shrimps crawled around her and she merely nudged them aside if they got too close. The team offered pieces of crab to her using a robot arm on their submersible; she turned them down. She may have occasionally grabbed nearby food or even eaten some of her own eggs, but the team found no evidence of this.

As the years went by, her condition deteriorated. When the team first saw her, her skin was textured and purple, but it soon turned pale, ghostly, and slack. Her eyes became cloudy. She shrank. And all the while, her eggs grew bigger, suggesting that they were indeed the same clutch.

View Images The female octopus brooding her eggs in April 2007 (a), May 2007 (b), May 2009 (c), October 2009 (d), December 2010 (e) and September 2011 (f). The black circle and white arrows show distinctive scars on her arms. Image copyright Robison et al, 2014. MBARI. CC BY 3.0

The team last saw her in September 2011. When they returned in October, she was gone. Her eggs had hatched and the babies within had swum off to parts unknown, leaving nothing but tattered and empty capsules still attached to the rock. Her body was nowhere to be seen.

This epic brooding period—53 months in total—is the longest known for any animal. The famous emperor penguin—a model of parental sacrifice—incubates its egg for just 2 months. The record-holder among octopuses was a captive Bathypolypus arcticus who guarded her eggs for 14 months. Among animals that raise their young internally, elephants do so for 21 months, frilled sharks for 42, and alpine salamanders for 48. The female G.boreopacifica that Robison observed beat them all.

How did the octopus survive for so long? Her inactivity and the near-freezing water certainly helped. Sitting mostly still at just 3 degrees Celsius, her metabolism would have slowed to a crawl.

This marathon of maternal care makes sense for a deep-sea octopus. The longer she keeps it up, the bigger her young can grow and the greater their odds for survival when they hatch. And since she dies after brooding is over, she might as well keep at it for as long as possible.

Indeed, G.boreopacifica lays unusually large eggs that give rise to unusually large hatchlings. The clutches are also very small—for comparison, the giant Pacific octopus lays clutches of around 100,000). These are all signs of a reproductive strategy called K-selection, where mothers invest more effort into raising fewer offspring.

It’s clearly a successful strategy since G.boreopacifica is a very common species. Perhaps a 53-month brooding period is exceptional only because we have never had a chance to measure these periods before. As the team wrote, “These results only seem extraordinary when compared with well-studied shallow-water species; which indicates how little we really know about the deep sea.”