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WHEN Charles Darwin set foot on the Galapagos Islands, he could look forward to finding five new species in as many minutes – a golden age of discovery that many biologists today can only yearn for. But for those of us exploring the “islands” of life on the ocean floor, it is still a reality.

At these lush islands, gushing chemicals feed communities of bizarre animals. Food chains here are based not on photosynthesis, but on a process called chemosynthesis, so the inhabitants of these vents should be indifferent to the changing seasons far above them and to global disasters that devastate life on the surface. “That party’s been going on down there in the dark for the past billion years,” says Hollywood director turned deep-sea explorer James Cameron in his recent documentary, Aliens of the Deep. “It’s got nothing to do with us. The sun could go out tomorrow and they wouldn’t know and they wouldn’t care.”

Or so people thought. But now a group of biologists (including myself) have found a thread linking these islands in the darkness with the sunlit realm above. Despite being far from the sun’s reach and having food enough to make merry all year round, some creatures down there still follow the seasons of the surface world. Their annual cycles hint that life in the oceans may be more connected than anyone realised – and that there may be nowhere to hide from the effects of climate change or an asteroid hitting Earth.

When marine biologists first encountered thickets of metre-long tube worms and beds of large clams around deep-sea hydrothermal vents in the late 1970s, their existence was baffling. Textbooks taught that all life depends on the sun: plants use energy from sunlight to make their food by photosynthesis, animals eat the plants and may get eaten themselves. But less sunlight reaches the deep sea than the surface of Neptune, so it was thought that all life in the depths depends on food that sinks from above. And the deeper you go, the less food there is, because it gets eaten en route. So at hydrothermal vents 2 kilometres or more beneath the waves, there shouldn’t be enough food to support such a riot of life.

Breaking the rules

But life at these vents breaks the rules, thanks to dissolved hydrogen sulphide and methane in the fluids erupting from the seabed. Microbes use the chemical energy in this cocktail to turn inorganic carbon into organic matter, in the same way that plants use light energy during photosynthesis. These chemosynthetic microbes form the base of the food chain, sometimes developing symbiotic relationships with animals.

With a home-grown food supply, life thrives around vents in an abundance that rivals that of shallow-water coral reefs. And chemosynthetic communities are not confined to vents, which are found only along the volcanically active mid-ocean ridge. They have also been found on the continental slopes at cold seeps, where non-volcanic processes push mineral-rich fluids out of the seabed.

Our exploration of deep-sea chemosynthetic life has only just begun.

The mid-ocean ridge stretches for 70,000 kilometres around the planet, dwarfing terrestrial mountain ranges. There are still vast sections along which hydrothermal vents are undoubtedly present but whose inhabitants remain to be discovered. Just a few months ago, researchers saw life at deep-sea vents in the Arctic Ocean for the first time (see page 40). New types of cold seep are also turning up, such as communities clustered around areas where hot tar flows from the seabed, found in the Gulf of Mexico in 2003. More than 600 new animal species have been described from vents and seeps so far, which works out at around one every three weeks.

As biologists started to study the reproductive habits of these species, few expected to find any seasonal patterns. Although a handful of species elsewhere in the deep sea reproduce seasonally, that pattern is linked to the bonanza of dead plankton that arrives from surface waters after algal blooms each spring. At vents and seeps, however, chemosynthesis provides plenty of food all year round.

The first hint that something seasonal might be going on at vents and seeps came in the late 1990s, when Susan Lisin at Monterey Bay Aquarium Research Institute and her colleagues noted that tissues in the ovaries of clams at a cold seep in Monterey Bay varied from month to month. Then in 2003, Gina Perovich at the University of Delaware in Lewes and her colleagues reported that crabs around a hydrothermal vent in the eastern Pacific showed signs of hatching their eggs in spring. These findings raised the possibility that life at vents and seeps might not be so divorced from the patterns of the sunlit world above after all.

A lake on the sea floor

My part in the story begins at the bottom of the Gulf of Mexico. In 2002 Craig Young of the Oregon Institute of Marine Biology in Coos Bay invited me to take part in a series of expeditions to the Brine Pool – a bizarre “lake” of ultra-salty water on the sea floor. The Brine Pool is a cold seep at which salt buried beneath the sea floor is pushing its way to the surface, forcing out methane trapped in seabed sediment. Seep mussels thrive on the methane bubbling from the pool, courtesy of chemosynthetic bacteria that live in their gills. And the mussel bed provides a home to other creatures such as shrimp.

I joined Young on several expeditions to the Brine Pool. We collected specimens in different seasons over two years using Johnson-Sea-Link submersibles. The superb all-round view from the two-person acrylic sphere of these subs makes them a favourite of deep-sea biologists. They are also well equipped for sampling, with manipulator arms, a hydraulic scoop and a suction sampler – an underwater vacuum cleaner that slurps specimens into sample jars.

In a visit in autumn, we found that most of the female shrimp at the Brine Pool, members of a species called Alvinocaris stactophila, were carrying recently spawned eggs on their back legs, suggesting that they had just reproduced. In early spring, we watched well-developed embryos from the shrimp hatch into tiny larvae aboard our research ship. When another batch of egg cells started to develop in the ovaries of shrimp collected in summer, the seasonal life cycle of the shrimp became clear. Meanwhile, Young and Paul Tyler at the National Oceanography Centre in Southampton found that the seep mussels follow a similar seasonal pattern, reproducing from October to February.

These patterns posed a puzzle: with food available all year round, why are these animals reproducing seasonally? The answer has to do with their offspring. Vents and seeps are islands, sometimes separated by large distances. The food supply of each island does not last forever, so their inhabitants release their larvae to drift in the currents to ensure that a few will reach and colonise new islands. Some larvae must feed during the trip, providing the link to the surface world that has been largely overlooked until now. The timing of reproduction is not controlled by the amount of food available for adults, but by the food available to their larvae. The springtime release of shrimp and mussel larvae coincides with a peak in the amount of food raining down from surface waters, giving the larvae a better chance of sustaining themselves while island-hopping. This seems to be the key to life at vents and seeps. “Without understanding dispersal, we’ll never understand the biogeography and maintenance of these populations,” says Tyler.

“With food available all year round, why are vent and seep animals reproducing seasonally?”

If this idea is correct, then species whose larvae do not have to feed on plankton should not reproduce seasonally. So far this prediction is holding up. Animals that send their offspring out into the world provisioned with yolk to sustain them, such as the famous vent tube worms, do not reproduce seasonally.

But do species that produce feeding larvae always reproduce seasonally? The answer is “not necessarily”. Not all areas of the ocean have seasonal blooms of algae, so species that live in the vents and seeps below them should not reproduce seasonally. This seems to the case for the shrimp Rimicaris exoculata, which swarms in great numbers around vents in the Atlantic and Indian Oceans.

Having found seasonal reproduction in the shrimp at the Brine Pool, I was keen to see if their cousins at vents followed the same pattern. Biologists tend to visit vents on the mid-ocean ridge in summer months, when the weather is better for dangling vehicles from research ships. But since I was looking for evidence of seasonal reproduction, I jumped at the chance to join a rare autumn expedition led by Rob Reves-Sohn and Susan Humphris from Woods Hole Oceanographic Institution in Massachusetts. Last November we set out on the research vessel Knorr, bound for a vent on the Mid-Atlantic Ridge right beneath an oligotrophic gyre, a circular current whose waters are low in nutrients. The result is the oceanic equivalent of a desert, with very few algae in surface waters all year round.

Despite a bumpy ride across the Gulf Stream, the weather did not hamper our dives with a remotely controlled submersible, Jason II, and we returned with an autumn sample of the vent shrimp. Back in the lab, the reproductive development of these shrimp proved identical to those in summer samples from the same vent. Some shrimp had very small developing egg cells, while others had very large ones, in contrast to the seasonally reproducing shrimp at the Brine Pool, which all had developing egg cells of very similar size in any season. So the vent shrimp do not appear to reproduce seasonally, at least at this particular hydrothermal vent.

Further north on the Mid-Atlantic Ridge, however, there is a seasonal bloom of algae in surface waters. And sure enough, there is some seasonality at the vents below. Ana Colaço of the University of the Azores in Horta and her colleagues are studying another species of mussel that lives at vents just south of the Azores. “The vent mussels have mature gonads in December and early January, and then they spawn,” she says.

Images from satellites show that this pattern ties in with a bloom of algae above these vents early in the year. So we can abandon the popular notion that life at vents and seeps is independent of the sunlit world above. And if what goes on in surface waters can shape patterns of life at vents and seeps today, could it have done so in the past?

Catastrophes such as the asteroid impact that contributed to the demise of the dinosaurs 65 million years ago may have blotted out the sun and disrupted photosynthetic life in the upper layer of the ocean. Palaeontologist Cris Little of the University of Leeds, UK, has put together a 430-million-year fossil record of life at vents and seeps and found that many of their inhabitants appear to have sailed through this mass extinction event unscathed.

But Little admits that the fossil record only provides a partial glimpse of life at vents and seeps in the past, as it is dominated by shelly animals that are more readily preserved. “If the bulk of the diversity is in soft-bodied worms, we’re never going to be able to say anything about that,” he says. “And we don’t have any record of crustaceans.” He is therefore open to the possibility that events affecting surface waters could have altered life at deep-sea vents and seeps. “There must be some sort of linkages because of the life cycles that we know so far,” Little argues. “In that respect they’re not entirely divorced from what goes on in the photic zone.”

Other, more gradual changes in surface waters might also be carried to these remote corners of the deep sea. Biologists are already starting to consider whether climate change may affect life elsewhere on the ocean floor. In the 1990s, David Billett of the National Oceanography Centre in Southampton, UK, and his colleagues noticed that herds of sea cucumbers had started to dominate the vast abyssal plain of the north-east Atlantic, after changes in the surface-water blooms. Climate change is one possible culprit.

“If it is related to the flux of organic matter to the sea floor, then global change in surface waters will be transmitted to the seabed within a matter of weeks,” warns Billett. Such changes could also be transmitted to vents and seeps, potentially altering the dispersal of some species between islands and hence the development of their communities.

“Global change in surface waters will be transmitted to the seabed within weeks”

The discovery of seasonality in the depths suggests that life in the marine realm is more interconnected than we had realised. I used to think that whatever havoc happens up here, the denizens of the deep would carry on regardless. Now it is becoming clear that although life at deep-sea vents and seeps will certainly survive whatever changes global warming brings, it may not survive unchanged.

For me, it is deeply satisfying to have been able to help discover something that we didn’t know before about how the world works, thanks to the most basic of scientific techniques: just by going somewhere new and measuring things, as Victorian scientists did. It’s reassuring and humbling to know that there are still plenty of places left on the planet where we can do this.