Slime, Shorebirds, and a Scientific Mystery

Could the survival of millions of migrating shorebirds depend on the preservation of humble marine biofilm?

Published November 15, 2016
Part of our 16 Best of 2016 series

As the tide pulls out over British Columbia’s Roberts Bank on an early October morning, it pools amid the hummocks, follows intertidal runnels seaward, and leaves a silvery-green sheen on the exposed mudflats where Canadian researcher Bob Elner walks. Thousands of southbound snow geese, propelled skyward by a hawk’s approach, move in ever-shifting murmurations to Elner’s right. Dunlin and ducks grub along the tideline to his left. But the western sandpipers, he observes, are gone. A scientist emeritus at Environment and Climate Change Canada, Elner has long studied the sandpipers, and he knows they have headed south on their 10,000-kilometer fall migration from the Arctic to Latin America.

The big unspoken question hanging over these mudflats is how long the sandpipers and other shorebirds will continue to stop on the Fraser River estuary and fuel up, before flying onward. Beyond Elner, as he struggles to maintain his balance on the treacherous mud, rise the silhouetted loading cranes of Deltaport, which lies at the end of a causeway jutting into the Strait of Georgia. Trainloads of coal (bound for Asia, Europe, and South America) and containers of manufactured goods (bound for Canada) arrive there every hour, 364 days of the year. Now the Vancouver Fraser Port Authority is proposing to double the container capacity of this facility by building nearby an entirely new island, called Roberts Bank Terminal 2, at a cost of more than CAN $2-billion.

Just what effect this mega development will have on the adjacent tidal flats and the sandpipers that flock here in the spring and fall is a point of contention in the environmental assessment that is now entering its final stages. At low tide, Roberts Bank—slime covered and sulfurous smelling—is a bleak expanse of shimmering, gray-brown mud. But the data that Elner and his colleagues have gathered here in the Fraser River estuary suggests that the sandpipers are extremely vulnerable if development proceeds. Indeed, the fate of these birds may now hinge on how regulators react to what Elner and his colleagues have learned.


In late April, flocks of several hundred thousand migrating western sandpipers a day refuel on the mudflats at British Columbia’s Roberts Bank. The future of the birds may be threatened by the Vancouver Fraser Port Authority’s Terminal 2 project, a proposed expansion of the shipping terminal just offshore. Photo by Matthias Breiter/Minden Pictures


Elner’s research on sandpipers began more than two decades ago in his office at the Pacific Wildlife Research Centre, located a kilometer and a half from the Fraser River estuary. A raconteur and maverick by temperament, Elner was working for Environment Canada and studying shorebirds, when a new shipping facility was proposed in the early 1990s at Roberts Bank. The new container terminal, Deltaport, was slated to go in beside the existing Westshore Terminals coal export facility, on an artificial island at the end of a five-kilometer causeway into the ocean.

Already, the causeway had begun impeding natural tidal flows on the southernmost flank of Roberts Bank, allowing eelgrass to spread over the muddy intertidal and subtidal zone. What effect would more construction have on the shorebirds? Elner happened to be studying one of the most numerous birds to migrate there: the western sandpiper. So he began looking in earnest into the relationship between sandpipers, their food, and Roberts Bank’s mud. How, he wondered, did these little shorebirds—no bigger than a human fist—acquire sufficient energy during brief migratory stopovers to take 1,000-kilometer-long transits without refueling?


The existing man-made island near the mouth of the Fraser River already hosts a coal terminal and a container terminal. In this artist’s rendering, the island on the left is the site of the proposed Terminal 2 project. It could double the container facility’s capacity. The sandpipers’ primary feeding ground lies between the proposed new terminal and the shore. Image courtesy of the Government of Canada, Asia-Pacific Gateway and Corridor Initiative

Examining the diet of western sandpipers during their layovers at Roberts Bank, Elner discovered, wasn’t easy. On the vast mudflats, the birds move incessantly, hyperactively, heads bobbing, beaks dipping into the shimmering slime on the mudflats’ surface, following the receding tide outward on spindly legs. Any approach sends thousands of birds airborne. Even through a telescope, it’s impossible to discern what they’re actually eating. So with a federal permit and a shotgun, Elner obtained several dozen sandpiper specimens to see what he could learn.

Today in his office, he extracts a collection of numbered glass vials from a cabinet and waves No. 104 in the air, its contents a clear liquid the color of sesame tea. “Ornithologists believed sandpipers ate little crustaceans, worms, and mollusks,” Elner says, sloshing more vials as he talks. “But the stomachs of the sandpipers were empty. Just this liquid, and some sand. Almost no crustaceans [or other prey],” he says. “It was a complete surprise. It didn’t make sense.”

So, if it wasn’t crustaceans, worms, or mollusks, the biologist thought, what were they eating that helped the northbound birds to fly nonstop until they reached the Stikine River estuary on the Alaskan panhandle?


Bob Elner has spent more than two decades observing migratory sandpipers on the 21,703-hectare estuary of the Fraser River. What he’s discovered there has revolutionized our understanding of the critical link between shorebirds and the mudflats on which they feed. Photo by Ron Watts

In the search for answers, Elner headed out, sometimes accompanied by a team of research assistants, onto the Fraser River’s slick tidal flats, often walking the southern swath that makes up Roberts Bank. The team struggled—like characters in Monty Python’s famous “Ministry of Silly Walks” skit—to keep their balance on the treacherous mud. There were days in late April, when several hundred thousand shorebirds—from dozens of species—filled the air in high-pitched, trilling clouds. Elner’s team would skim the veneer of slime from the mud’s surface, collect sandpiper poop for evidence of nutrients, and try to document the birds’ feeding patterns.

“We spent hundreds of hours watching them,” Elner recalls. “We noticed the sandpipers arrive regularly at the same time every year.” They seemed to prefer the southernmost intertidal mudflats at Roberts Bank, as opposed to other parts of the Fraser River or delta. But he had no idea why. “We also saw—as the tide went out—some shorebird species kept following the retreating tideline all the way out. But the sandpipers went 300 meters out, and stopped.” The birds knew something, but Elner didn’t know what that was.

To find out exactly what, he turned to Peter Beninger, now a professor of marine biology and ecology at the Université de Nantes in France. In his lab, Beninger had a powerful scanning electron microscope capable of magnifications of up to 300,000 times. Elner shipped off several sandpiper heads to Beninger in 1997, to see if microscopic study could reveal something about the birds’ feeding habits. The first thing Beninger noticed was that, unlike many shorebirds that feed exclusively by probing tidal flats for crustaceans and mollusks with their beaks, western sandpipers have feathery tongues, whose edges and tips are covered with keratinous bristles. Could these be used like a mop, he wondered, for slurping up the silvery gunk on the surface of the tidal flats—a substance scientists call biofilm?


As the tide recedes from the vast mudflats of Roberts Bank, millions of northbound shorebirds find nourishment each spring for the next leg of their journey to the Arctic. Each flight between stops can be more than 1,000 kilometers. Photo by Ron Watts

Beninger shifted the microscope to 1,000-times magnification. There embedded in the bristles were tiny, single-celled algae called diatoms. With silica-glass cell walls, diatoms are crystalline, almost jewel-like, and plentiful beyond number. More importantly, they are carbohydrate-rich and therefore essential to marine ecosystems. They provide energy and vital nutrients for zooplankton and in turn—moving up the food chain—for as much as half of all ocean life. “This was our eureka moment. We couldn’t believe it,” says Elner. “The sandpipers appeared to be eating diatom-rich biofilm.”

Even today, Elner can barely contain his delight at this discovery. He laughs aloud. “Snot. Biofilm. Mucous. Saliva. It’s all the same thing: microbial goo. Energy-rich goo. It had never been reported before. It looked like the birds were eating slime.”

This “goo,” says Elner, is ubiquitous, and develops naturally in very thin, opalescent layers, in varying concentrations, on intertidal mudflats worldwide. It’s composed primarily of single-celled bacteria and diatoms, and a mucous-like carbohydrate that bacteria and diatoms produce to bind individuals together. The protein also allows the bacteria and diatoms to bond with the mud’s surface, ensuring that the microbes remain unaffected by the ebb and flow of tides. Within this sticky, organic matrix, the photosensitive, single-celled diatoms thrive.

BioFilm_Animation-FINAL

This short animation explains how biofilm forms on the mudflats, and how the western sandpipers slurp it up with their special bristly tongues.

Leading ornithological journals, however, were skeptical. Elner and Beninger’s findings contradicted conventional wisdom. Every shorebird study, every birding book said that migration-bound sandpipers ate crustaceans, worms, and mollusks. For two years, the scientists tried to publish their findings, but no academic journal seemed interested in a report saying that western sandpipers, and their dunlin sandpiper cousins, ate biofilm from mudflats to fuel their flights. It was too bizarre. It couldn’t be true.

But the two researchers didn’t give up. “We knew what we’d discovered was important,” Elner says. “It posits a rethink about the value of biofilm and mudflats to birds.” So the two researchers decided to go outside the field of ornithology, and send their paper to a journal called Marine Biology in 2004. It came out with the title: “Evidence of a new feeding mode in western sandpiper (Calidris mauri) and dunlin (Calidris alpina) based on bill and tongue morphology and ultrastructure.”


It was an important step forward, but the two researchers still needed corroboration from others, who could independently confirm the hypothesis elsewhere. Out of the blue, Elner heard from Tomohiro Kuwae, a Japanese biogeochemist and intertidal flats ecologist now at Japan’s Port and Airport Research Institute. His job, he explained to Elner, was to assess the biology of the intertidal flats and the foraging habits of shorebirds on the east coast of Tokyo Bay. He was collecting this data, in part, to understand the impact of nearby industrial and port activities. Perhaps, Kuwae suggested, they could work together?

Kuwae knew from his own and others’ research that migratory bird populations taking the so-called East Asian-Australasian Flyway—an aerial avenue used by tens of millions of shorebirds each year during their transits along the Asia-Pacific coast—were in serious decline. Numerous species, including spoon-billed sandpipers and eastern curlews, had been put on endangered or vulnerable lists. In fact, populations of several wading species, including wood sandpipers and dunlins, were down 30 percent. The causes seemed obvious. The growth of urban populations and booming economies have destroyed the shorebird habitats in more than 40 percent of all major river estuaries along the coastline of China and South Korea.

When Kuwae arrived at Roberts Bank in 2004, he brought with him a new technology that would turn the question of sandpiper diets into a major environmental issue, one of global significance. With a video camera equipped with a telephoto lens, he planned to record the rapid tongue and bill movements of sandpipers. When viewed frame by frame, the video would reveal whether the sandpipers were purposefully eating mudflat slime. Kuwae also planned to analyze biochemically both the Roberts Bank biofilm (with its embedded diatoms) and the birds’ stomach contents and droppings for their respective caloric values. This would allow him to calculate how important biofilm was to sandpipers’ diets.


This map shows the location of Roberts Bank and the existing Deltaport terminal in the Fraser River delta. It also highlights the adjacent swath of mud and biofilm that may be affected. Western sandpipers that land at Roberts Bank feed on biofilm and prefer to stay within about 300 meters of the shore. Illustration by Mark Garrison

When Elner and Kuwae sat down together to watch the slow-motion video of the sandpipers’ feeding, they could clearly see the beaks open and the feathery tongues flick out, slurping up the paper-thin surface layer of mudflat slime like thirsty dogs at their water bowls. “It was mind-blowing,” Elner says. What he and Beninger had contended was correct: the sandpipers were purposefully eating biofilm.

Months later, Kuwae appeared at Elner’s office door with the biochemical findings, which he described as “very exciting.” The Japanese researcher and a small team had used toothbrushes to meticulously collect biofilm samples from various locations and at various times on the Fraser River estuary. The subsequent analyses of these and samples from the birds showed that biofilm accounted for as much as 59 percent of the birds’ diet.

As Elner spent more time on Roberts Bank, he noticed that the slime, rich in bacteria and diatoms, covered the entire Fraser River estuary, but seemed to be unevenly distributed. Although the picture varied throughout the year, a lot of biofilm occurs within the nearshore 300 meters or so of the tidal flat. There in late April, under a warm spring sun, trillions of the plant-like diatoms began reproducing. And as they bloomed, they produced—through photosynthesis—massive amounts of fatty acids. It was a huge seasonal pulse in fat production, and the sandpipers seemed to capitalize on this. Taken together, the findings of Kuwae, Elner, and Beninger revealed just how dependent the birds were on diatoms rich in essential fatty acids. Biofilm provided more than calories. It was what western sandpipers used to build endurance for their long migrations, and stay healthy en route.


The Pacific Flyway is a chain of stops along the west coast of North America that’s used by more than a billion migrating shorebirds each year. Many of the key stops are major river estuaries with mudflats where the birds feed. As this map shows, many are also sites of potential, proposed, or ongoing developments that can impact the quality of that food. If the chain of stops is broken, birds are unable to migrate and breed, and entire species can be at risk. Illustration by Mark Garrison

Elner thought the implications of this work were ground shaking. The findings could explain why the birds arrived each April precisely when they did, and why they—as he’d previously observed—only used the nearshore sections of Roberts Bank for feeding. That was where the diatoms were most available to the birds in the Fraser River estuary. And if sandpipers were feasting on this choice food on Roberts Bank, he thought, they were likely doing that in other estuaries on their migration routes. And probably other shorebird species were dining on it too. Biologists had noted that one subspecies of red knot, a type of sandpiper that migrates along North America’s east coast, arrives at Chesapeake Bay estuaries each year at the precise time that female horseshoe crabs come ashore to lay their fatty-acid-saturated eggs.

Mudflats, Elner realized, could be essential to the future of migratory shorebirds. During their long spring migration, western sandpipers, for example, often stop to feed on tidal mudflats in coastal estuaries. But many people think of these flats as an ecological wasteland, prompting developers to target them. And that means Kuwae’s findings could have real political implications. Deltaport began operating in 1997. But in 2011, the Vancouver Fraser Port Authority resurrected plans to double the capacity of the shipping facility on Roberts Bank by building Terminal 2.


News of Elner and Kuwae’s sandpiper investigation reached San Francisco’s John Takekawa, director of San Francisco Bay programs for the National Audubon Society and a specialist in documenting the movements of migratory birds. His goal, he explains, is to better understand—using advanced telemetry—the mysteries of bird migrations in order to conserve their populations. To that end, he had information to add to Elner and Kuwae’s findings. At Takekawa’s research base in the southernmost part of San Francisco Bay—an area with 16,200 hectares of tidal flats—he and his associates had been gluing tiny, one-gram transmitters onto migrating sandpipers’ backs, devices that fall off within a month. Each transmitter has a frequency code that allows researchers to identify the specific bird and its location along its flight path between its over-wintering regions in North and South America and summer breeding grounds in the Arctic.


Together with scientific associates in France, Japan, and the United States, Bob Elner discovered that the organic biofilm on the mud’s surface is essential for sandpipers’ migratory flights. Photo by Ron Watts

Takekawa’s findings now reveal what happens during the sandpipers’ epic flights. Refueling at estuaries on their annual spring migration to Alaska, the sandpipers—each weighing about 25 grams, less than a single chicken egg—fly nonstop as many as 500 to 1,000 kilometers north of that day’s departure point. Moving, if winds are favorable, at 50 kilometers per hour, an individual sandpiper might use the same sections of a dozen or so Pacific coast estuaries each spring. And Takekawa lists the most important ones: San Francisco Bay, Roberts Bank, Alaska’s Stikine River estuary, and the Copper River Delta in southeastern Alaska. He likens these to “a necklace of stops” that, if broken by industrial construction, real estate development, or an oil spill, could seriously impact migrating bird populations. When the birds arrive hungry and exhausted at each estuary along the chain, refueling is critical. If any one stop is removed, he now wonders, could the shorebirds die?

What started as a mystery more than 20 years ago has led both Elner and Kuwae to publish a series of scientific papers—the most recent by Kuwae in 2015—which continues to shed light on what many now believe is a major scientific discovery. Pat Baird, a research associate at Simon Fraser University’s Centre for Wildlife Ecology, in Burnaby, BC, has spent years in migratory bird studies. She knows all about estuary ecology and biofilm and has studied the research on the diatom-sandpiper connection. “What Elner has learned,” she says, “was never known before. It’s a new paradigm. It’s huge.” Strong circumstantial evidence, she adds, suggests that sandpipers and other shorebirds probably eat diatoms to fuel up for their long-distance flights in many other estuaries in the world.

And Peter Beninger, the French expert on electron micrographs, says of the new research on mudflats: “Scientifically, this is one of the most significant developments in ornithology in the past century.”


As Elner stumbles up to his SUV parked atop the sea dike that separates the Roberts Bank salt marsh from the farmland to the east, he’s laughing. He pulls off his hip waders and seeks a rag to wipe away the viscous black muck that clings to his hands and elbows after a fall during his latest foray onto the tidal flats. Once again, the mud has tripped him up. But, after more than two decades pursuing a mystery, Elner now knows its secret.


Slick and slippery to walk on, the mud at Roberts Bank lacks the visceral appeal that many other environmental battlefields have, such as old-growth forests. But debate is growing over the future of this vital area. Photo by Ron Watts

Just offshore, the moored container ships, loading cranes, and coal trains of the Roberts Bank shipping terminal rumble in a low, visceral growl. What will happen next out there is uncertain. The Terminal 2 project is currently undergoing an environmental assessment, with a final decision on whether it will proceed due from the federal government in 2017 or 2018.

The ridges of the distant Gulf Islands to the southwest, and the more distant ridges of Vancouver Island, are the colors of faded denim. A freighter moves north along the Georgia Strait. Chevrons of honking snow geese move south. “What we’ve got,” says Elner, “is entire species whose future rests on what we’ve learned. This has global impact. It’s the same here as along the southeast Asia flyway where there’s already a loss of huge numbers of shorebirds. Mud’s not like classic old-growth forests: places that people easily get. People say: ‘Oh, it’s just mud. What’s the problem?’ It’s not just mud. It’s essential. We need to protect those places where biofilm and diatoms thrive. The loss of mudflats means the loss of whole flyways. The loss of species. Millions and millions of birds.”