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When Snails Attack: The Epic Discovery Of An Ecological Phenomenon

By Christie Wilcox
Aug 27, 2018 1:00 PMMay 21, 2019 6:00 PM
Amos Barkai discovered this now classic example of predator-prey reversal 30 years ago. Photo used with permission from Amos Barkai
Amos Barkai discovered this now classic example of predator-prey reversal 30 years ago. Photo Credit: Paul Hanekom (used with permission from Amos Barkai)


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The year was 1983. Star Wars: Return of the Jedi had just hit theaters, The Police’s “Every Breath You Take” topped the charts, and Amos Barkai was a new graduate student at the University of Cape Town in South Africa. He’d recently gotten his bachelor’s from Tel Aviv University, and was excited to start his graduate work under George Branch. Little did he know he was about to discover an ecological phenomenon that would earn him a prestigious paper in Science.

Branch had been investigating the effects of bird guano runoff from islands on life in the intertidal—the zone between high tide and low tide—and he was interested in seeing whether the effects extended into deeper waters. Since Barkai was an experienced diver (he’d worked as a professional diver for the Israeli Navy and as a commercial diver after that), Branch sent him 100 kilometers or so away to Saldanha Bay, a protected coastal kelp ecosystem. “I packed him off to one of the islands we’d been working on, callled Marcus Island,” Branch explained. “I told him, You’re fully qualified as a diver, so I want you to go and do some exploratory dives. Take a look around there, and see if you can see anything interesting.”

It just so happened the area was experiencing a once-in-a-lifetime storm with waves over 18 meters high. “I didn’t know I was exposing him to hell on Earth, and he came back completely shell-shocked,” said Branch. “I think he wondered what kind of supervisor he was getting involved with.” But once things calmed down a bit, Barkai did get in the water, and looked for evidence that the birds nesting on Marcus and other nearby islands were affecting the communities near shore. He didn’t find any—but he did notice something strange.

Near to Marcus was Malgas Island—so named for the gannets, a kind of seabird, which nest there (Malgas is old Dutch for “mad geese”)—which looks entirely similar to Marcus Island from the surface. The seabed, however, told Barkai a very different story. Although they’re just a few kilometers apart, the species he saw “were strikingly different,” he said. West Coast Rock Lobsters (Jasus lalandii) or ‘kreef’ as they are known locally were everywhere around Malgas. Several hundred of them per square meter crowded into crevices and under ledges—there was “basically nothing else.” To find anything that wasn’t a lobster, he had to peek under the holdfasts connecting the kelp to the substrate. There, he found mussels and a few Burnupena papyracea—small whelks (a kind of marine snail).

Around Marcus Island, though, “the bottom was covered with anything but lobster,” Barkai said. A dense mat of mussels lined the benthos, and it was decorated with whelks, sea urchins, and sea cucumbers galore, but nary a lobster to be seen.

Further studies at Malgas revealed that the lobsters were so abundant that there was fierce competition for food. “The lobsters were basically fighting for everything that was there. The only thing that usually survived was sponges and seaweeds,” Barkai said, and whatever could hide beneath the kelp. As soon as a juvenile mussel or barnacle tried to settle down, the lobsters scraped it up and ate it. “The lobsters were dominating the benthos,” he explained. 

To see what would happen if these lobsters were removed, Barkai put in protective cages with mesh too small for the lobsters to enter. “All other species started to flourish,” he said. “It was clear the lobsters were responsible for the deficit of most life at Malgas Island,” Branch noted.

So… what was different about Marcus? The two islands are so close together, and other than a breakwater connecting Marcus to the mainland, there didn’t seem to be any obvious explanation for this stark difference in the numbers of lobsters. Barkai measured currents, did some sample collection, looked at benthic — or seafloor — structure, but nothing really stood out as an explanation for the vastly different assemblages of species. He and his colleagues even threw a few lobsters in a cage and showed they could survive just fine in the waters at Marcus. The diverse buffet at Marcus should be an irresistible to any lobsters able to find their way there—so why weren’t the hordes at Malgas making the short trip over to feast?

After consulting with Branch, Barkai decided to conduct an experiment—”a very naive and not really well thought out idea,” as he now describes it. He planned to take about a thousand lobsters from Malgas and move them to Marcus to see how they fared.

On the day of the experiment, Barkai was alone in the water, as he was working with a topside crew that didn’t dive (something that would make university dive safety officers extremely uncomfortable nowadays. Of course, this was the ’80s, and things were different). First, the boat stopped at Malgas, and Barkai collected the lobsters for the transfer. A short 4 kilometer boat ride later, and both he and the lobsters entered the waters by Marcus. And that meant he was the only one to witness what happened next.

“Visibility was great that day, and virtually the entire sea bottom started to move,” he said.

That movement was countless whelks. They started to climb onto the newcomers, sticking to their legs. “I didn’t know then, but they’d started to suck them alive, basically. It was like a horror movie,” Barkai said. “It actually was a bit frightening to watch.” The lobsters simply didn’t know how to respond. They were outnumbered and overwhelmed.

“To my horror, in about 30, 40 minutes, all the lobsters were killed.”

"It was horrifying," said Barkai. "It was actually a bit frightening to watch." Photos used with permission from Amos Barkai

“It was horrifying,” said Barkai. “It was actually a bit frightening to watch.” Photos used with permission from Amos Barkai

Barkai managed to bring two whelk-coated lobsters back to the surface to show the crew—which is when the first photo in this piece was shot. The bewilderment on his face says everything. On the ship, they carefully pulled the whelks off—over 300 per lobster. “When we removed the whelks from the lobsters, they were empty shells. There was no meat left at all whatsoever. They were simply empty shells,” he recalled. “Basically the only thing that kept them together was the whelks, so the moment we removed the whelks, the lobsters just fell apart.”

But perhaps the most awful part was seeing up close how the whelks had done the lobsters in. They had penetrated every single soft tissue that they could find with their tubular mouthparts—the lobsters’ eyes, joints, anywhere with even a little give. “You could see these very long pipes coming in from the inside of the lobster,” Barkai explained. The poor lobsters—”they didn’t have a chance.”

When he told his advisor what happened, Branch was dumbfounded. “I actually said to him, You know, you must have done something wrong,” Branch recalled. The results were just too unbelievable. 

The pair quickly realized that the ravenous whelks—an animal normally on the lobster’s menu—were why Marcus Island had no lobsters. “That was absolutely shattering, because here was a complete reversal of a normal predator-prey relationship,” said Branch—and the paper that resulted, published in Science in 1988, was the first study to document such a reversal. 

The caging studies at Malgas had shown that these predatory whelks and other species happily flourished in the absence of lobsters, but they didn’t explain why there weren’t lobsters at Marcus to begin with. So Barkai dug into the history of the two islands, and he learned that Marcus actually was a lobster paradise once—just 20 years prior. But that was before the bay was a marine reserve, and Marcus’ connection to land made it a popular lobster fishing ground. He suspects that the lobsters there were overfished, essentially to local extinction. With lobsters out of the picture thanks to fishermen, everything else was free to settle and grow unencumbered. And they did, until there were so many whelks that the lobsters could not come back.

And it wasn’t just that the whelks became too numerous—they had an ally against any hungry lobsters that might have happened upon them. Barkai had noticed that in this area, this particular species of whelk was covered in an encrusting bryozoan (a somewhat coral-esque animal). He and Branch’s former PhD student, Christopher McQuaid—who was then a postdoc at the University of Cape Town—worked together to show that this bryozoan was protecting the whelks. In feeding experiments, the lobsters generally avoided whelks with the bryozoan on their shells, but happily consumed them if the shells were scraped clean. “It was a much more complicated story than we initially thought,” explained Branch. “Yes it was true that whelks were excluding lobsters. But it is probably also true that they could only secure that ascendancy because they were protected by this bryozoan.”

Branch and Barkai soon realized they were looking at strong evidence for alternative stable states—the somewhat controversial idea that an ecosystem can exist in very different yet completely stable configurations. “A lot of scientists are skeptical,” said Branch, but further studies on the islands have made a convincing case. Barkai is no longer involved personally in the research—not long after he obtained his PhD, he left academia, though he remains tied to the ocean as the Director for OLSPS Marine, a company that specializes in fisheries data management (he still lives in South Africa, but he said the last time he got in the waters of Saldanha Bay was nearly two decades ago). But Branch (now an emeritus professor at the University of Cape Town) and his colleagues conducted surveys in 2016, and little has changed. “Malgas Island is still dominated by lobsters,” Branch said. “Their numbers are not as great as they were, but nonetheless, there are still large numbers there… And Marcus still has huge numbers of whelks and no lobsters.” So the two very different ecosystems have proven stable for more than 30 years.

And the evidence for alternative stable states continues to mount. After he published the findings in Science, Barkai said he was flooded with researchers noting similar predator-prey reversals, especially involving whelks. “In many fishing grounds, when you don’t have lobster, you get many whelks on the bed instead. So it’s obvious that there is some kind of interaction between the two species—the two species are sort of competing between themselves,” he said. Research in the decades since has also found other incredible examples of predator-prey role reversals, and it’s become clear that they may be more common than previously thought.

Barkai and McQuaid’s findings can also provide insight into the repercussions of a much more recent phenomenon: the sudden proliferation of lobster in the fishing grounds known descriptively as “East of Cape Hangklip.” Before 1989, the area was essentially devoid of lobsters. “Historically, lobsters were regarded as a west coast species in South Africa,” explained Branch. That all changed in the early 1990s. “They had increased very radically to the south, creeping around the tip of the Cape peninsula onto the south east coast,” he said, and by 1995 or so, “the south east coast had accumulated large numbers of lobsters in an area where they had been very rare before.”

And when the lobsters moved in, they took over the benthos, exerting top-down control of the community just like they have for decades as Malgas, Branch’s student Laura Blamey found. “She was able to make comparisons over time by comparing before they invaded and after they invaded, and over space, by comparing areas they had invaded with areas they hadn’t invaded,” Branch said, and she found that in areas now sporting lobsters “things like urchins and mussels and limpets… they’d all been been enormously depleted.” Invertebrates other than lobsters declined by 99.3%, according to Blamey’s research. And once that happened, the algae those species usually kept in check grew unabated. “Kelp abundance increased hugely,” Branch said—by 453%, to be precise.

It might not sound terrible to have more lobsters around, especially since the population on the west coast is currently struggling. Kreef have declined dramatically due to overfishing and have even been recently listed as endangered. And fishers certainly took advantage quickly—the lobsters are now fished heavily in their new southeastern territories.

But the expansion of the lobster fishery has come at the cost of an even more lucrative one: abalone. Another one of Branch’s  students, Elizabeth Day, found that the urchins the lobsters have essentially wiped out are key to the survival of juvenile abalone. “The urchins are sheltering places,” Branch explained, where young abalone can hide until they’re large enough to fend off many of their predators. When urchins disappear, so, too, do young abalone, Day’s research found. “If you remove the urchins, very quickly, the numbers of juvenile abalone crash,” Branch explained. And that means the abalone are getting a double whammy—”the adults are being decimated by poachers, and… the survival of the juveniles is being diminished by the removal of urchins by lobsters.”

Meanwhile, on the western coast, the lobsters have found a way to persist at low densities. So far, Branch said he hasn’t found anywhere where things have shifted the other way—from lobsters to whelks—which is “very surprising”, given that the lobster population is a mere 2.6% or so of its former glory. Barkai was never able to repeat the scale of his experiment (perhaps unsurprisingly, he was unable to get permits to move thousands of lobsters after what happened), so it remains unknown how rare the lobsters must become—or how abundant whelks with their bryozoan bodyguards have to be—before the marine snails are able to turn on their crustacean predators. It’s probably a good thing that such a shift hasn’t happened yet, though, because it’s not clear how to undo this kind of role reversal—or if that’s even possible. There simply isn’t a roadmap for reintroducing lobsters to areas dominated by whelks.

Still, even if the lobsters are keeping the whelks at bay for now, the possibility of a shift to snail-covered seabeds looms as the battle over the west coast lobster fishery heats up. For now, limiting or even halting lobster fishing altogether could help lobster populations bounce back—which is why the World Wide Fund for Nature – South Africa (WWF) faced off in court last week against the Department of Agriculture, Forestry and Fisheries (DAFF) over the total allowable catch limits for the iconic seafood. WWF is arguing that the limits are too high, and that DAFF is ignoring scientific advice—a charge the government disputes.

If WWF’s efforts fail—and they’re right about the catch limits being too high—then the lobsters will become even more scarce in years to come. And if that happens, then Branch and other ecologists in South Africa just might get the chance to learn what it takes for the whelks to take over.


Citation: Bakai & McQuaid, 1988. Predator-Prey Role Reversal in a Marine Benthic Ecosystem. Science, 242(4875): 62-64. DOI:10.1126/science.242.4875.62

And for those who noticed: No, it’s not a coincidence that the embedded tweets come from a “Branch”—Trevor Branch, a professor at the University of Washington, is George Branch’s son.

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