Science (pg. 678), May 4, 2007


[Rachel's introduction: Besieged by pathogens, predators, and people, the "rainforests of the sea" may soon face their ultimate foe: rising ocean acidity driven by CO2 emissions, says the American Association for the Advancement of Science.]

By Richard Stone

KHURA BURI, THAILAND -- In the shallow waters off Lan Island in the Andaman Sea, Kim Obermeyer kicks his flippers and glides over a silent graveyard. Scattered below are shards of staghorn and other branching corals, shattered in fragments that look like detached finger bones. The conservation biologist swims farther out to sea, darts to the bottom, and peers under an overturned Porites coral head the size of a Volkswagen Beetle. Obermeyer points to a brown ribbon underneath: a ragged colony soaking up just enough sun to have survived the tsunami that struck on 26 December 2004.

As a horrific tragedy unfolded on shore that day, ecosystems below the ocean's surface were getting hammered. Across Southeast Asia, the titanic waves ripped apart shallow reefs and buried others in silt. But tsunamis are not the worst threat. The main menaces are largely human-wrought: from divers clumsily breaking off chunks of coral to mass die-offs and bleaching of coral triggered by spikes in ocean temperatures. Last month, the Intergovernmental Panel on Climate Change (IPCC) forecast "more frequent coral bleaching events and widespread mortality" with average global temperature increases of 1 deg. to 3 deg. C.

Surveys suggest that 20% of the reefs on Earth, the largest living structures on the planet, have been destroyed in the past few decades. Another 50% are ailing or verging on collapse. "Reefs are likely to witness a significant ecological crisis in the coming half-century -- because of us," says coral specialist Camilo Mora of Dalhousie University in Halifax, Canada.

The decline of coral reefs may have staggering consequences. Globally, reefs generate about $30 billion per year in fishing, tourism, and protection to coasts from storm surges, says Mora. Although reefs cover a minuscule fraction (0.1%) of seabed, they are second only to rainforests in biodiversity, sheltering or nourishing up to 9 million species -- a third of all known marine life forms -- including 4000 kinds of fish. "To predict that reefs will change dramatically across the globe in the matter of a single generation should keep people up at night," says Ove Hoegh-Guldberg, director of the Centre for Marine Studies at the University of Queensland in St. Lucia, Australia.

There are a few rays of light in this bleak seascape. Attempts to rehabilitate tsunami-damaged reefs are showing promising results. Some reefs blighted by bleaching have mounted spectacular comebacks. And efforts to limit fishing and human activity have paid dividends in healthier reefs and revived local fisheries. Over the past decade, hundreds of marine protected areas have been established to safeguard reefs, including innovative MPAs in Palau designed to help corals bounce back after bleaching (see sidebar, p. 680).

Yet these gains could be erased by what's shaping up as the gravest threat of all. As the oceans soak up more and more of the carbon dioxide that humans pump into the atmosphere, marine chemistry is changing. CO2 emissions "have the potential to create chemical conditions in the ocean that have not occurred since the dinosaurs became extinct," says ecologist Kenneth Caldeira of the Carnegie Institution of Washington in Palo Alto, California. Dissolved in water, CO2 becomes carbonic acid. Caldeira coined a term for this process in a paper in 2003: "ocean acidification." By midcentury, ocean pH could dip so low that corals would be unable to form their calcium carbonate skeletons.

"Acidification is the big elephant in the room," says Terence Hughes, director of the Australian Research Council's Centre of Excellence for Coral Reef Studies at James Cook University in Townsville, Australia. Reef building would grind to a halt, with grievous implications. If CO2 emissions are not curtailed, Hughes predicts, "we'll eventually see reefs dominated by sea anemones and algae." Put another way, "soon we'll be having jellyfish and chips," says biologist Michael Kendall of the Plymouth Marine Laboratory in the United Kingdom. In the darkest scenarios, most corals will be toast.

A multiheaded monster

As coral reefs slip toward chronic frailty, a picture of what this means to the world has begun to emerge. Coral scientists, backed by an army of snorkeling and diving volunteers, have put a watch on critical reefs among the nearly 300,000 square kilometers charted to date. Hidden gems continue to come to light, including a giant deep-water reef in turbid waters off northern Australia. "Not much is known about the reef because nobody wants to swim in that area. It's infested with crocodiles," says oceanographer Alan Strong, senior consultant to the U.S. National Oceanic and Atmospheric Administration's (NOAA's) Coral Reef Watch.

A recurring theme of this heightened scrutiny is that reefs are vulnerable on many fronts. A March 2005 earthquake off Indonesia, for example, was as brutal as the 2004 tsunami, lifting some reefs clear out of the water (Science, 20 October 2006, p. 406). Corals are susceptible to pathogens and predators, too. The crown-of-thorns starfish, a periodic invader, denudes coral outcroppings with the efficiency of a slash-and-burn farmer. Meanwhile, corals are perpetually besieged by filamentous algae, which are held in check by fish that nibble at them. Overfishing can tilt the balance, as can sewage or agricultural runoff, which infuse seawater with algae- feeding nutrients. These abuses, along with coastal development, "are having fantastically large and negative impacts on reefs around the world," says John Pandolfi, a coral reef expert at the University of Queensland in Brisbane, Australia.

The latest and perhaps biggest present danger for reefs is bleaching. When sea surface temperatures exceed their normal summer high by 1 deg. C or more for a few weeks running, coral polyps, for reasons not entirely understood, expel their zooxanthellae, the symbiotic algae that lend corals color and provide nutrients. The polyps turn pale and starve. "If they don't get their zooxanthellae back in a month or so, they die," says Obermeyer.

The dangers of bleaching came to the fore in 1998, when a potent one- two climate punch -- a strong El Nino warming in central tropical Pacific waters, followed by a La Nina that heated western Pacific regions -- killed 16% of living corals worldwide (Science, 27 October 2000, p. 682). Some reefs have rallied from severe bleaching -- recently and dramatically, off Darwin Island in the Galapagos. "We'd given up on the Galapagos" after a 1982-83 bleaching event annihilated most of the archipelago's reefs, says Strong. Now, he says, "it seems to be really coming back." However, many bleached reefs are still sickly. At least half of those destroyed in 1998 have not recovered, according to the authoritative Status of Coral Reefs of the World: 2004, compiled by the Global Coral Reef Monitoring Network (GCRMN).

The catastrophic 1998 bleaching, and regional occurrences since then, highlight the vulnerability of reefs to global warming. "That's when we realized that corals could be a kind of canary in a coal mine," says Jeremy Goldberg, co-author of a GCRMN report on tsunami-inflicted reef damage. Delicate staghorn and elkhorn corals, for example, were listed as threatened in the Caribbean in May 2006 under the U.S. Endangered Species Act. "Branching corals that are sensitive to bleaching might disappear," warns reef ecologist Thamasak Yeemin of Ramkhamhaeng University in Bangkok.

Some reefs are more tolerant to bleaching. However, says Hoegh- Guldberg, "the movement toward hardier communities of fewer coral species is hardly a 'win.' " Coral abundance is still plummeting, and even resistant corals may succumb in a warmer world, he says. "As climate change accelerates, we will lose an increasing number of coral species, making ecosystems less resilient to other pressures."

A case in point is the widespread bleaching in the Caribbean Sea in 2005-06. At one reef off St. John, part of the U.S. Virgin Islands, "before people knew it, a disease infected the coral that had survived the bleaching. What was left was totally wiped out," Strong says. "You can see how this gets to be a multiheaded monster." NOAA and U.S. National Park Service scientists are now searching for clues to why some corals survived whereas others perished.

In an attempt to boost reef survival, governments have been setting up MPAs, which range from free-for-all recreational parks to no-take zones that bar fishing. Fewer than 3% of the world's reefs lie inside no-take MPAs, says Mora. Many reefs are being fished out. Raising the specter of a pending food crisis, a recent study found that 27 of 49 island countries are exploiting their reef fisheries in an unsustainable way, reports a team led by Nicholas Dulvy of the Centre for Environment, Fisheries, and Aquaculture Science in Lowestoft, U.K., in the 3 April issue of Current Biology.

Lax enforcement and lack of local buy-in have undercut many MPAs. "If communities are not involved, they are very unlikely to support an MPA imposed on them," says Obermeyer, coordinator for Reef Check Thailand. With volunteers from Reef Check and a second nonprofit, Earthwatch, Obermeyer endeavors to involve villagers -- and here near Khura Buri, the Ranong Coastal Resources Research Center of Kasetsart University -- in reef monitoring. "This is the only way to succeed," he says.

MPAs and measures such as stanching sewage and runoff cannot prevent bleaching. But resilience -- the capacity of a reef to absorb recurrent bleaching and still function -- can be enhanced, Hughes says. In 2002, more than half of Australia's 40,000-square-kilometer Great Barrier Reef bleached. Two years later, Australia created the world's largest no-take zones, extending fishing bans covering 4.6% of the reef to more than 33%. "This initiative provides real insurance cover against the inevitable impacts of climate change," says Hoegh- Guldberg.

To test this approach, Hughes and colleagues caged some reef sections and left others open to grazing by parrot-fish, known by their fused, beaklike teeth. Polyps reestablished on open reef three times faster than on caged sections, they report in the 20 February issue of Current Biology. The study shows that reef management after bleaching "has a big effect on the recovery rate," Hoegh-Guldberg says. But the strategy works only in the short run; nations must move rapidly to stem greenhouse gas emissions, he says. "It is next to useless not to do the two things together."

A mortal blow?

Until bleaching reared its head, many experts viewed rising sea levels as the chief peril of global warming for coral -- and a relatively toothless one at that. "We thought reefs would respond by just growing higher," says Strong. "Nobody was talking about changing sea chemistry." Then researchers came to the creeping realization that rising ocean acidity is likely to throw a spanner in coral physiology.

The threat is glaringly simple. Currently, ocean pH hovers around 8.1. Carbon dioxide absorbed into the water column lowers the pH, and as it falls, fewer carbonate ions are available for shell-building critters to grab. Even in present conditions, corals are fighting an uphill battle: Erosion removes 80% of the calcium carbonate laid down. Acidification will accelerate that process as rising carbonic acid levels deplete carbonate. Eventually, corals, plankton, and other organisms will fail to form skeletons. And coral skeletons are to reefs what girders are to skyscrapers. "You have a potential world in which reefs and the limestone frameworks they have built are in net erosion," says Hoegh-Guldberg.

IPCC scenarios of global emissions and ocean circulation indicate that by midcentury, atmospheric CO2 levels could reach more than 500 parts per million, and near the end of the century they could be above 800 ppm. The latter figure would decrease surface water pH by roughly 0.4 units, slashing carbonate ion concentration by half, paleocoral expert C. Mark Eakin, coordinator of NOAA's Coral Reef Watch, testified last month at a hearing in the U.S. House of Representatives. Ocean pH would be "lower than it has been for more than 20 million years," he said. And that does not factor in possible acidification from carbon- sequestration schemes now being considered.

Some coral species facing their acid test may become shape shifters to avoid extinction. New findings indicate that corals can survive acidic conditions in a sea anemone-like form and resume skeleton-building when returned to normal marine conditions (Science, 30 March, p. 1811). However, by pH 7.9, says Caldeira, "there would be a good chance reefs would be gone."

The potential for an acid-induced coral cataclysm has cast a pall on the tight-knit community of reef specialists. "The reality of coral reefs is very dark, and it is very easy for people to judge coral reef scientists as pessimists," says Mora. "We're becoming alarmist," adds Strong -- for good reason, he insists. "How are reefs going to handle acidification? It's not like sewage or runoff, where you may be able to just turn off the spigot." Queensland's Pandolfi, however, argues that it's "too early to make really definitive doom-and-gloom statements."

No one disputes that urgent action on greenhouse gas emissions is essential. "We could still have vibrant reefs in 50 years time," Hughes says. But these will not be the reefs we know today. "They will be dominated by a different suite of species," says Hughes, who notes that the shakedown is already under way.

More likely, steps to rein in emissions will be too little, too late -- and the world will have to brace for the loss of reefs. In Southeast Asia, says Hoegh-Guldberg, the threat of millions of people losing their livelihoods must be factored into policy planning. Coastal dwellings throughout the tropics will have to be strengthened against higher waves. Then there is the intangible, aesthetic deprivation if coral reefs wither and wink out. "Without their sheer beauty," Hughes says, "the world would be an impoverished place."

Copyright 2007 American Association for the Advancement of Science