ARE ALL SPECIES EQUAL?
ROBERT T. PAINE was a giant, not only because he towered above six feet but also because he made such significant scientific contributions. After completing his postdoctoral research at the Scripps Institution of Oceanography, he took a faculty job at the University of Washington in Seattle. I met Bob shortly before I became a professor at Scripps myself, in 1999. He told me how a little experiment changed his life—and ecological science—forever.
Bob had been a student of Fred Smith at the University of Michigan. He remembered one class when Smith pointed to a tree on the university campus and asked his students why it was green. “Chlorophyll” was the easy answer: the pigment in leaves that helps extract energy from the sun. Yes, chlorophyll gives leaves their green color, but why are there even leaves on this tree? Why don’t the caterpillars eat them all? They seem like such an abundant supply of food! Smith’s more sophisticated answer to his question was that the world is green because herbivores don’t consume all plant material, since predators keep the herbivores in check. That is, caterpillars are not as abundant as they could be because birds eat them. That idea later became known as the “green world hypothesis,” and it made Bob think about the role of predators in shaping our environment.
In 1963, Bob was a new professor at the University of Washington, and he was looking for a place to study what predators do to the ecosystems they inhabit. He discovered the Pacific shore and its intertidal zone, the region that is bathed by the rising tide and then dries during the low tide. It represents a symmetrical boundary between sea and land. The marine creatures living there have an abundant supply of water rich in nutrients every six hours, but they also emerge and have to survive out of water for hours at a time. The boundary between the sea and the land comes and goes, rhythmically. Living at the edge of two worlds has its pros and cons.
Bob found that the intertidal zone of the Washington shore was rich and productive, with large abundances of algae and invertebrates, such as anemones, sea urchins, limpets, barnacles, mussels, sponges, and a distinctive sea star, Pisaster ochraceus. P. ochraceus is purple and orange, with five arms, thick and curved like a bodybuilder’s. Bob called that ecological community his nirvana. Like a good naturalist, he spent countless hours in the field, acquainting himself with the species living there and observing who ate whom. He would turn sea stars and sea urchins over to see what was on their mouths, note what type of barnacle a snail was attacking, and watch mussels open their shells as the tide came in, loaded with plankton.
Bob focused on the food web at Makah Bay, a three-and-a-half-hour drive west of Seattle, where he found sea urchins and limpets eating algae, snails eating barnacles, and P. ochraceus at the top of the food web, eating mussels and almost every other invertebrate. He wondered what would happen if he removed the top predator. Bob looked at a sea star, and after some thinking, he picked it up and threw it to deeper water. That was the moment that would change Bob’s life, experimental ecology, and my life as well.
Bob threw another sea star to deeper waters, and another, and so on. He depopulated a single outcrop of sea stars in a nondestructive way. (The sea stars survived in deeper waters.) But he also left other areas untouched, as controls. That’s the way scientific experiments work: Manipulate the factors you want to understand in one treatment, maintain the same factors without change in another, and then compare the outcome. Medical researchers call this a randomized controlled trial, and it is a sine qua non of scientific research. If we manipulate something in nature and want to know what the effects are, we need to compare it with an unmanipulated control. We also need to conduct manipulations in several different areas, or experimental plots, alongside several control plots.
Bob would drive to his study site to hit the low summer tides, clean the outcrop of P. ochraceus, make measurements of the abundance of different species in the experimental plots and the control plots, and drive back home to Seattle. “After only a year and a half,” he said, “I knew that I hit ecological gold.” So what had happened?
When sea stars were removed, nobody was there to eat the mussels. Therefore, the mussels could expand, occupying more of the intertidal rock. But other species were living there and occupying that rock. Fortunately for the mussels, they had a competitive advantage (like the Paramecium aurelia in Gause’s test tubes that dominated over P. caudatum): They could overtake other organisms. And so they did, overgrowing and smothering everything else. For creatures that live attached to the bottom of their environment and survive by filtering seawater, as mussels do, space is everything. And in the absence of predators, mussels gained the competitive advantage for space.
In only a year and a half after the removal of Pisaster ochraceus, the intertidal community went from 15 different species to eight. And in seven years, the whole intertidal zone turned into a monoculture: Mussels were the only species left, having pushed all other species out. Those results were surprising, though. You would expect that removing the top predator, the P. ochraceus sea star, would increase the abundance of everything else below them.
To ensure that P. ochraceus was indeed special, Bob removed other species from the community. But he found the effect of removing others very small. As George Orwell wrote in his book Animal Farm, “All animals are equal, but some animals are more equal than others.” In ecological terms, that means that not all species have the same impact on the community they inhabit. Bob’s simple experiment proved, for the first time, that a single species—Pisaster ochraceus—can determine the composition of an entire ecological community. Shortly after, Bob published one of the most important papers in ecological science, proposing the idea of a “keystone species” and showing that P. ochraceus is a keystone species in the intertidal ecosystem he had been studying.
In architecture, the keystone is the stone in the middle and at the top of an archway that keeps the arch together and standing: Remove it, and the whole structure collapses. Remove P. ochraceus, and the whole structure of the intertidal ecosystem goes away. Bob defined a keystone as a species that has an effect on the entire ecosystem, not just on the species that it eats. And the impact of a keystone species is disproportionately greater than its abundance. That is, a predator is a keystone species when its abundance is relatively low—but its per capita effect is going to be disproportionately high. Few but powerful. Remove that species, and the community changes dramatically, typically becoming much simpler, with less diversity.
Most known keystone species are top predators, but there are species that aren’t at the top of the food chain that still have a tremendous influence on the ecosystem. What are they, and how can they help us understand how human activities are changing the natural world?
ANOTHER GIANT of American experimental marine ecology, Paul Dayton, did his doctoral work under Bob Paine’s supervision, also studying the intertidal zone off the coast of Washington State. He found the time to start a scientific diving program in Antarctica, too, in heroic times where he and his buddies conducted an aggregate of 500 dives, wearing old wet suits in waters at minus 1.5°C (–29.3°F). Today we dive in those waters inside dry suits and wearing three layers of technical underwear!
Paul was based off McMurdo Station, one of the scientific bases run by the United States. There was concern that the permanent human presence, together with the pollution caused by activities on the land, ice, and sea there, would have a detrimental effect on the previously pristine ecosystem. A great naturalist and ecologist, he first tried to understand the organization of the ecological community in the bay. He quickly realized that studying the effect of pollution on each species in the community separately would take a long time and a great deal of funding. Measuring the effects of pollutants on the interactions of all the species in the community would be impractical, especially in an environment where divers cannot stay submerged for more than half an hour at a time, even when wearing a wet suit, because of the unforgiving pain caused by the frigid waters. He had to come up with a shortcut.
Thus Paul thought that he should identify the species that have a disproportionately important influence on the structure of the community. Once they were identified, it would be easier to consider the effects of the pollutants or other disturbances on them, and thus indirectly on the rest of the community. For these Paul introduced the definition of “foundation species,” but he clearly distinguished foundation species from keystone species. What’s the difference? One of the best examples came from Paul’s later research.
After obtaining his Ph.D. at the University of Washington, Paul went to work at Scripps, where he started the longest running study on giant kelp forests. Giant kelp is the redwood of the sea, its long strands like pillars starting as deep as 120 feet and reaching all the way up to the surface, sometimes growing a foot and a half a day. Every kelp is anchored to the bottom by a cone-shaped mesh of holdfasts from which dozens of stems, called stipes, arise. Gas-filled bladders about the size of large olives dot the stipes, which are crowned by broad, leaflike blades. Giant kelp continues to grow even once it reaches the surface, creating a canopy atop the water’s surface through which sunlight filters as if through the stained glass of a cathedral. I have to admit to having a soft spot for Paul and his kelp forests, because once I moved to Scripps, I conducted research on kelp under his supervision.
Giant kelps provide the architecture of an entire ecological community. Their intricate holdfasts are inhabited by hundreds of worms, crustaceans, sponges, and many other creatures. Their blades are covered by little tube-forming worms and other invertebrates. Just beneath the kelp forest is an understory of smaller kelps, together with fleshy and coralline red algae, amid which sea urchins, abalones, and snails make their living. Like birds in a terrestrial forest, fish inhabit the giant kelp forest at all levels, some specializing in eating shrimplike creatures living on the kelp stipes, some grazing the algae of the understory, and others—such as the imposing black sea bass—eating every other fish in the food web. The giant kelp is the foundation species for this entire community: It provides the conditions for the diversity and abundance of species. Remove the kelp, and most other species go away.
Therefore, foundation species provide the structural basis of the ecosystem—its physical habitat—whereas keystone species keep the ecosystem going. Keystone species can be few and powerful, with a large influence on their ecosystem, but foundation species tend to be numerous and omnipresent. Just a few P. ochraceus sea stars (keystone species) can regulate the structure of their intertidal community, but it takes many kelp plants (foundation species) to form a kelp forest with its full complement of species.
One might then ask: Can there be keystone and foundation species in the same ecosystem? How do they interact with each other, and what are the implications for the ecosystem?
Back in the 1960s, Bob Paine had observed that intertidal pools at Tatoosh Island in Washington State were full of sea urchins, which had eaten all of the kelp. Bob saw there a clear violation of Smith’s green world hypothesis: Here was a place where herbivores did denude all their plant prey. So he did what had worked so well for him in the past: He removed all sea urchins from some pools and left others untouched. The results were almost immediate. In the pools without sea urchins, kelp started growing fast. But he still questioned why sea urchins were naturally so abundant there.
Another scientist, Jim Estes, would be touched by serendipity—and Bob’s influence—and come up with the answer. Jim is another tall and impressive scientist, handsome and soft-spoken. He was studying sea otters in Alaska, furry marine creatures that are the epitome of cuteness. Jim had met Bob at a bar (this is not a joke) and had told him about his intention to conduct a study on the physiology of sea otters, considering how energy flows in the Alaska ecosystem, from the kelp all the way up the food web to sea otters and larger species such as orcas. Bob, after listening to Jim, told him he did not find that idea too interesting, and asked whether he had thought of understanding what otters do to the system instead. One could try that by replicating Bob’s species removal experiment. But how do you remove sea otters from some kelp forests while keeping them in others?
A thriving sea otter fur trade had started in the mid-1700s in Alaska, and that had wiped out most of the otters from the region. But a few survived, and laws passed to protect sea otters in 1911 helped to replenish the species along the Alaska coast. Some islands, like Amchitka, which Jim knew well, had recovered their sea otters. At Amchitka, sea urchins were common but very small, and kelps were abundant.
But then Jim dived at Shemya Island, where otters had not come back for some reason. “The most dramatic moment of learning in my life happened in less than a second, and that was sticking my head in the water at Shemya Island,” Jim said years later. “It was just green with urchins and no kelp.” The underwater world of Shemya looked like Bob’s pools in Tatoosh: The dominant herbivore—the sea urchin—had removed all its prey—the kelp. And without the kelp, all other species were gone as well, including the otter.
Sea otters love to eat sea urchins, and so Jim realized that the absence of otters had likely caused the explosion of urchins. He had found another keystone predator: In this community, it was the sea otter, at the top of a food chain formed by otters eating sea urchins eating kelp. Sea otter removal had caused indirect effects throughout the food web, from carnivores to herbivores to plants. Bob Paine had called those indirect effects in the food web “trophic cascades”: situations where predators control the structure of the ecosystem from the top down.
Twenty years later, Jim was having a hard time finding otters in Alaska; they seemed to be declining, and he also had a hard time finding a plausible explanation. There was enough food, so starvation could not be a cause. And they did not show signs of disease. But a colleague of Jim’s, Brian Hatfield, met him at Amchitka Island one evening and told him that he had seen an orca attack a group of otters. Jim was skeptical. Orcas—killer whales—are the most formidable predator in the ocean, eating everything that’s large, including whales, Steller sea lions, and even the feared white shark. Large animals, especially those with a high concentration of fat in their tissues, are a preferred item in their diet. No way would they be eating candy when they could be eating steaks. But Hatfield saw another attack at precisely the same place the next day. The following winter Jim’s technician, Tim Tinker, also saw orcas eating otters at Adak Island.
Clam Lagoon, Alaska, provided another extraordinary natural site for an experiment. The bay had a narrow entrance, narrow enough to allow sea otters to come in and out but too tight for orcas. Jim and his colleagues found abundant sea otters in the bay, even though in nearby areas, orcas were common. Jim had found another keystone predator, a longer trophic cascade, and an extraordinary story of indirect effects, but in this case, it would turn out to be humans who were at the top of the food web, causing unexpected changes across ecosystems and decades.
Alan Springer of the University of Alaska, Fairbanks, envisioned an intriguing hypothesis to explain the otter-orca phenomenon. After World War II, Japanese and Russian whalers started killing whales on an industrial scale. By the late 1960s, they had removed nine out of 10 whales in the North Pacific. (Orcas were too small to be of any harvest value, and thus their numbers were not directly diminished by industrial whaling.) A type of orca also specialized in killing large whales. The hunting of large whales offshore triggered a cascade of changes: Without large whales to prey on, those orcas had to move closer to shore and eat other species. Orcas first went after harbor seals—smaller than sea lions but fatter and more energy rich. When they had depleted the harbor seal population, they started eating sea lions, and when there were few sea lions left, sea otters. As the sea otters dwindled, their prey—the sea urchins—thrived, eating away the kelp and creating barrens, stripped of all the animals that a healthy kelp forest supports. As Jim said, “The amazing part of that was the notion that something like whaling that started in the middle of the 20th century, way out in the oceanic realm of the North Pacific, could affect something like urchins and kelp in the coastal ecosystem. It was mind-blowing…almost like science fiction.”
WHEN I WAS AN UNDERGRADUATE at the University of Barcelona in the 1980s, I learned about Bob Paine’s, Paul Dayton’s, and Jim Estes’ studies. The type of work they did appealed to me, combining time in the field, experimentation, and ecological theory. I was an avid diver who could not get enough time underwater. Most of my early diving, after I turned 18 and was legally allowed to scuba dive, took place in the Costa Brava in Catalonia. I was used to a sea with clear water, a few small fish, and an ocean floor turned into a barren because of the grazing activity of too many sea urchins—like at Shemya Island in Alaska. And then I did my first dive in the Medes Islands Marine Reserve, where fishing was prohibited, close to the border between France and Spain. There I saw what Jim saw in Shemya, but in reverse: Inside the reserve there were lots of large fish, sea urchins were rare, and little algal forests covered the bottom.
The subject of my Ph.D. thesis was settled: I would study the effects of removing predatory fish, using the marine reserve and the unprotected areas nearby as the site of my natural experiment, and I would conduct experimental removals to test the impact of the predators. I spent hundreds of hours underwater. I scraped samples of the miniature algal forest and the hundreds of little creatures within, later identifying and counting them under a microscope. I counted fish and sea urchins while diving. I observed what the fish ate and installed plastic cages underwater to control the predation factor so that fish could not access their prey. And I spent hours simply watching what was going on around me. After three years of fieldwork, my data revealed a story similar to that of my scientific heroes. Where fishing was prohibited, the fish were abundant and the ecological community was thriving. Everybody was there: big and small fish, algae, and all the smaller species that thrive in the same ecosystem—and even sea urchins, but not too many, and hiding. Where the fish had been removed by fishing, the sea urchins had proliferated, eating the algal forest away and leaving a barren seafloor. A trophic cascade in the Mediterranean.
I found that predators not only reduce the abundance but also change the behavior of their prey. The Mediterranean shallow rocky bottoms go through the seasons, just as the land does. In the winter, seawater temperatures drop to 12°C (53.5°F). Days are short and algal abundance is low, but as the days lengthen and seawater temperature increases through spring and summer, the ecosystem flourishes. Algae grow fast. Miniature forests expand to as much as a foot in height, sometimes containing more than 100 different types of algae in an area no larger than a dinner plate. During the warmer months, the boulders in the Medes Islands Marine Reserve wore a biological wig of sorts, a healthy tuft of brown and red algae that covered all but the bottom third of the boulder. It was as if a barber had shaved the base of the boulders. What was the reason for that pattern, I wondered?
Looking more closely, I saw sea urchins tucked inside the space between the boulders and the seafloor. Maybe they were responsible. During the day, with all the predatory fish swimming around, these sea urchins were hiding. What happened during the night, when most fish were resting? There was only one way of knowing. I returned at night and dived on the boulders. As predicted, the large fish were nowhere to be seen, but at the base of the boulders, sea urchins had now come out from under and were grazing on the algae growing nearby, creating halos that extended about a meter around each boulder. A meter: That’s the distance a sea urchin was able to crawl at night before having to return to hide during daylight hours. Similar halos have been observed in other ecosystems, such as in Caribbean seagrass beds. There, sea urchins graze out circles around patch reefs where they shelter from predators during the day and conduct feeding excursions at night.
Everywhere we look, we find the same pattern: When the predators are there, their prey is less numerous and more scared. It’s a landscape of fear, but the community is more diverse. Remove the top predators, and the ecosystem collapses.
Field biologists have found this in temperate forests, where the presence of wolves makes their deer prey spend less time eating in the open, thus fostering the growth of forests. In grasslands, grasshoppers are more wary and eat less grass in the presence of spiders, thereby enhancing grass growth. In pristine coral reefs such as Kingman Reef in the Line Islands, I have seen plenty of sharks swimming around but few of their prey, which I found to be hiding among the corals during the day. In lakes, predatory large-mouth bass control the abundance of minnows that eat zooplankton; the minnows spend more time hiding from the bass, thus their zooplankton prey abounds, in turn controlling the abundance of phytoplankton—thus making lake waters crystal clear. Similar examples are found in ecosystems across our planet.
The conclusion is unavoidable: If we want a diverse and rich world, we need to keep the predators there. Keystone predators are particularly important, and most fragile. They are the fewest in number and yet the species with the strongest impact on their ecological communities. They also tend to be the first species that humans eliminate from an ecosystem when they show up: wolves, sharks, sea otters.
But not only the keystone species are important; so are the foundation species, which provide the architecture for the entire community. Often species sit in the middle of the food web, but their presence can also be critical. Take the example of the long-spine sea urchin (Diadema antillarum) in the Caribbean.
Decades of overfishing in the Caribbean meant fewer large fish, including the large parrotfish that eat algae and the triggerfish and porgies that eat adult D. antillarum. By the 1980s, D. antillarum were incredibly abundant, with average densities of 10 urchins per square meter in Jamaica. A voracious eater of algae, D. antillarum kept their growth in check, so the coral reef stayed healthy, dominated by corals.
But in 1983–84, D. antillarum suffered a mass die-off across the Caribbean, caused by an as yet unidentified disease. Hurricanes and increased nutrient runoff from agriculture fostered blooms of large brown algae amid the coral reefs. In decades past, parrotfish and surgeonfish would have controlled the algae. With them gone, D. antillarum was the last significant herbivore—a species that maintained a delicate balance within its ecosystem. After the sea urchin die-off, though, the large brown algae had no predators, hence they overgrew and smothered the coral, putting another nail in the coffin of Caribbean reefs.
THANKS TO THE WORK of passionate field ecologists like Bob Paine, Paul Dayton, and Jim Estes, we are beginning to understand the importance of a few large species in their roles as keystone or foundation species. Unfortunately, we don’t know what most species do, though. It would be impractical to perform the thousands of experiments that would be required to determine the impact of every species in its community. But one thing we do know, as Bob said: “To ignore the fact that there are top-down effects is to invite mistakes.”
One way to think of the role of species in their communities is to think of them as having ecological jobs. Using our analogy of the city, New York probably has thousands of different jobs, from mayor to pizzamaker to pet hairdresser. Each has a different role and impact within the community—the urban equivalent of species within their communities. Can we live without some species? Well, it depends on what their role is. To return to the city analogy: If all the canine stylists in New York City went away, some ladies on the Upper East Side would be upset, but the city would continue working perfectly well. If the garbage collectors went away, though, it would result in disease and social unrest, eventually leading to societal catastrophe.
It’s not as easy to make the same sort of value judgment among species in nature, however. One of them could be that quiet ecological keystone, gluing ecosystems together—the one species whose removal causes the whole community to collapse. Another species could be providing a service that is essential to our survival—just as do many insects, unknown to us, as they pollinate the trees that produce the fruits we eat.
As Bob Paine said years ago, all species may be equal, but some are more equal than others—and we don’t yet know which ones. But we do know that for millennia, humans have been removing top predators from the natural world. That impulse has simplified our world, because top predators tend to be the glue that keeps ecosystems together. It’s only relatively recently that we have started to learn that all ecosystems on Earth are linked to one another in ways that may appear magical—because they are.