Where the Wild Things Were

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by William Stolzenburg

No more dead stuff for Robert T. Paine. Remembering his Harvard days contemplating interactions of four-hundred-million-year-old fossil shells, Paine soon found himself standing shin deep in Alligator Harbor, watching the live versions in active battle. There were eight of them: Pleuroploca gigantea, Fasciolaria tulipa, Fasciolaria hunteria, Busycon contrarium, Busycon spiratum, Murex florifer, Polinices duplicatus, and Sinum perspectivum—otherwise known to any amateur collector by such names as Florida horse conch, tulip snail, lightning whelk, shark’s eye moon snail. But these were something other than a benign collection of shiny shells in a museum display case. In life, all were working predators. And all were earnestly involved in eating each other.

  Inside these crawling ornaments beat the hearts of pure predators, wielding single-minded intents and one of the meaner pieces of weaponry in the animal kingdom. All slugs and snails of the molluscan group known as the gastropods come with a muscular strap of tooth-studded flesh called the radula. It is a tool in various forms analogous to the workman’s rasp, file, drill, and chain saw, the critical distinction being that the radula is most often employed to destroy and consume living flesh. Among the carnivorous clan of gastropods, the radula is commonly wielded against its cousin snails and clams. Plowing through the sandy bottoms, the hunting snail bumps against another shell, and the struggle begins. If the defender comes with an open-ended shell, such as another snail, the process is straightforward and quick. The attacker’s proboscis snakes its way inside and the eating commences, rasping away at the hapless homeowner cornered in its own fortress. If the prey is a clam or mussel, valves tightly closed, the radula emerges to begin the slow work of drilling through the shell. It may take two days to penetrate, but the snail has patience, working the drill slowly from this angle and that, like a diamond bit through rock. Once the shell is pierced, the proboscis pushes inside, and the radula goes to work on soft flesh, shredding the clam where it lives. What remains when the snail leaves is an empty clamshell with a clean circular hole, as if pierced by a bullet.

  Some snails dispense with the precise drilling in favor of brute force, prying their proboscis through an unguarded opening. If the opening is too small, they chip away at it with a sharp edge of their own shell until the proboscis fits. And then again the radula finishes the job.

  This was the brand of carnage Paine had come to witness. Inside this outwardly meek world of the mollusk, Paine was spectator to a vicious society of pursuit and piercing wounds, gang-tackling, winner-take-all contests of strength, breaking and entering, piracy, and cannibalism. Paine would walk these sandy battle shores and methodically tally the casualties, marked by drill holes and chipped shells, sometimes catching predation in the act. In the end he would note the winners and losers, who were eating whom. In the end, big uncommon shells were eating small and numerous shells—a pyramid of predators.

  It was all so very Eltonian.

  For better or worse. These, like Elton’s seabird observations, were just that. They were not experiments; they were observations. They showed only that big shells ate smaller shells. There was no accounting for how the individual acts translated to numbers lower on the food chain. They proved nothing about why the world was green. HSS was still just a balloon of a theory waiting to be either bronzed or popped by experimental evidence.

  In order to truly test how much the top predators held sway, one would have to do more than watch; one would have to dive in and start moving pieces around, to manipulate the predators, to measure the before’s and after’s, the with’s and without’s. For starters, one would need a system a bit more tractable than the confounding gang of little predators trolling Alligator Harbor.

  “The Dumbest of All Experiments”

  In 1961, Paine defended his dissertation to a committee including Nelson Hairston and Fred Smith, the first two thirds of the infamous HSS. Finishing up at Michigan, he again headed for the coast, this time to the Pacific sands for a stint of postdoc research at the Scripps Institute of Oceanography in La Jolla. There he studied a sea slug that ate other sea slugs—“Just sucked ’em in! An absolutely violent act.” It was molluscan mayhem all over again. It seemed that everything was coming up predators for Paine.

  In his free time, Paine would venture down to the Scripps wharf, where he found clinging to the pier pilings massive beds of California mussels. And they in turn were under attack, by leagues of ochre starfish. Paine dwelled upon the scene.

  Mytilus californianus, the California mussel, is a blue-gray bivalve, cousin to the clam, with the competitive advantage of a secreted fiber cable called the byssal thread, by which to anchor itself on hard surfaces. The byssal thread is one large reason for the extensive range of the inadequately named Mytilus californianus, a creature of surf-exposed rocks and pier pilings from the shores of Alaska to Baja.

  Mytilus eats by opening its shell and straining plankton from seawater. Snuggled tight against its neighbor, lazily yawning to its belly’s delight, apparently commanding the life of Riley, Mytilus does occasionally suffer enemies. Shorebirds and crabs will take advantage of a mussel in a vulnerable moment. Big whelks will sometimes drill their way through Mytilus’s shell. These it takes in stride. But if a mussel could feel fear, Mytilus would be positively quaking in its shell at the approach of one Pisaster ochraceous.

  Pisaster, less formally known as the ochre starfish, is big and brawny, its arm span reaching eighteen inches in some of the giants of the race. It is a hardy, shallow-water species, capable of withstanding strong ocean surges, big swings in temperature, and desiccation when left stranded by the tide. Like Mytilus, Pisaster has mastered life over the rocky breadth of the North American Pacific coast. Unlike Mytilus, Pisaster is pure carnivore, and mollusks are its favorite meat.

  With high tide, Pisaster comes hunting, creeping out of the depths, up the pilings, up the rocks, to where the mussels have huddled. Gliding about on thousands of tiny hydraulic feet, Pisaster gives chase at speeds better appreciated with time-lapse photography, yet infinitely faster than any rock-bound mussel. Upon bumping into the prospect of prey—the starfish being essentially blind—Pisaster crawls on top, tiny tentacled feet sniffing for the scent of food. Edibility thus determined, the starfish centers itself over the mussel and stands it up, hinge-side down. The mussel is now positioned so that if it were to sneak a peek, it would be staring straight into the mouth of Pisaster. The starfish embraces the mussel, envelopes it like a tent. Its arms clamp around the opposing shells and begin prying.

  The pull is not explosive, but steady and unyielding. It is the ratcheting squeeze of a python in reverse. It is less a matter of grip strength than endurance. Mytilus’s muscles begin to tire. A tiny gap opens between valves. The fight is lost.

  Pisaster exploits the opening, injects a dose of stomach juice into the gap. The weakening mussel is being digested where it lives. The opening widens, and in comes Pisaster with its entire stomach. Extruding its gut out its mouth and into the home of Mytilus, Pisaster begins feeding externally. Two days later, depending on portion size, the starfish leaves a vacant shell and crawls on to another.

  The preceding explanation implies a Pisaster free-for-all. But in practice, there is a bit more cat-and-mouse to the contest. A starfish prowling much beyond the low tide line—up where the masses of mussels lie huddled—is an exposed and vulnerable starfish. Crashing waves can batter and dislodge it. The attacking starfish advances at its increasing peril. Too long out of water, its hydraulics begin to falter, and a strong and stubborn mussel gradually gains the upper hand. Both starfish and mussel are vitally tethered to the sea by invisible chains, but it is the mussel that is able to endure a critical step higher up the tide line.

  On the Scripps wharf, Paine stood before this cobbled pavement of orange starfish humped over doomed mussels—Pisaster chewing on Mytilus—and experienced, in his words, “Love at first sight.”

  He pried off a starfish to ponder the mussel smothered in its lethal embrace. It struck Paine that he
could intervene in the predatory act as easily as walking up and plucking a starfish. He began to sketch an experiment, as one might a theatrical play. He already had in hand the Pisaster-Mytilus dynamic, his lead predator and prey. He penciled in a few clams, some crawling gastropods, a few worms to play supporting roles in his ecosystem. Now he would measure the predator’s power in the most logical way—he would remove it. He would remove Pisaster from an intertidal community and see how everyone else in the food web fared.

  “It was clearly the dumbest of all experiments, removing starfish to reveal some idea of how their prey would respond,” said Paine. “It just struck me as bizarre that nobody had thought to remove Pisaster to see how Mytilus would respond. To see how the system worked. What roles the species played, rather than just their addresses.”

  This was territory that even his hero Elton hadn’t quite explored. As rock-solid as Elton might have been in his reasoning—who would argue that the greenery beneath the seabird cliffs of Spitsbergen had not been fertilized by fish-eating birds?—without systematic experimentation, his observations still amounted to conjecture.

  Paine’s sketch grew into a full-blown proposal. He would find his model community and test its vital structure. And away he went, with his first professorship awaiting him at the University of Washington in Seattle and a prestigious grant from the National Science Foundation to carry out this important new investigation on the role of predation in the web of life.

  There was only one small catch. The only place Paine knew for sure to find his concocted ecosystem was still on paper.

  Playing God in a Tide Pool

  Paine arrived at the University of Washington in 1962 and went to stake out his study plots. He searched the shores of the San Juan Islands, to the far ends of Puget Sound. No luck. He knew his creatures existed, he knew from the literature they indeed lived together. He just couldn’t find them.

  As it happened, part of Paine’s teaching assignment included a field trip to the coast, a four-hour drive west from Seattle to the tip of the Olympic Peninsula. In May of 1963, he led his students to a remote beach of rock and sand for their introduction to the natural history of marine invertebrates. And there on the rocky shore of Mukkaw Bay, he saw it laid out in front of him, waiting. My god, here it is right in front of my eyes, thought Paine. “It took me half a millisecond to say, ‘Wow, this is what I’ve been looking for.’” A month later, Paine was back, chucking starfish, embarking on one of the classic studies in community ecology.

  Twice a month, Paine would travel from campus in Seattle, board a ferry across Puget Sound, and drive the long coastal road heading west, tracking the Strait of Juan de Fuca toward its meeting with the Pacific. Approaching the tip of the Olympic Peninsula, he would cross into the Makah Nation, where earlier in the century Makah tribesmen hunted gray whales with harpoons thrown from canoes dug out of cedar trees. Then he would make a short inland jaunt across the peninsula, to the coast of the Pacific and the little cove of Mukkaw Bay.

  Mukkaw Bay forms an arc of dark sand and rock, where the face of the continent is still being freshly ground. At the northern tip of the arc, the Pacific Ocean and what used to be headland of the Olympic Mountains are still at odds. There standing in the water is a sea stack, quintessential landmark of the Northwest coast, a naked pillar of stone still defying the surf. And lying beside it is a rubbled tongue of rock, still struggling to keep its nose above water with every incoming tide. Here, according to the scriptures of ecology, lay holy ground.

  There were no beach stands, no umbrellas, and for the most part, no people. Paine would walk to the outcrop, a labyrinth of rock walls and channels surging with water on the incoming waves—a flooded badlands. It was a place of beauty, of pools glimmering with multicolor gardens of red and brown kelp and green anemones, pink coralline algae and purple sea urchins, yellow tunicates and blood stars.

  The rock was pitted and grooved, the seascape constantly changing with the pendulum swing of the tides and thrashing storms. It was this ironic harshness—these rocks to hold on to; these shrouds of fog and pools of wetness providing refuge against the desiccating exposure of low tide; this turbulent influx and flush of marine nutrients—that gave the rocky shore its vitality.

  It was a good place to cling, providing you came with the suction feet of a starfish, or the anchoring cables of a mussel. It was something more the treacherous place if you were a tall, two-legged creature evolved upon African savannas. Over this terrain the six-foot, six-inch Paine invariably came weaving and bounding, twice a month in spring and summer, once in winter. He set up his study on two adjacent twenty-five-by-six-foot sections of rock, featuring a ledge to stand on and a handily accessible wall of marine animals exposed by the tide. Here he had all the ingredients for deciphering what a community ecologist would formally characterize as a Pacific Northwest intertidal food web.

  The rock was a stratigraphy of marine life. Near the top clung scattered clumps of little acorn barnacles, they in turn interspersed with clusters of the big and beautiful goose barnacle, intricately cloaked in harlequin shells. Below the barnacles formed a blue-gray band dominated by the California mussel, packed ear to ear.

  In the tidal pools below, the neighborhood suddenly flowered into a marine melting pot—two species of Chinese hats called limpets, four species of variously colored algae, a big green anemone, a sponge, and a sponge-eating slug called a nudibranch. And separating one from the other, oddly contrasting midway up the rock, was a constellation of big orange and purple starfish, Pisaster ochraceous.

  The pecking order was well established, and starkly simple. Pisaster fed on all shelly creatures of the rock; none fed on Pisaster. In this kitchen-size ecosystem, Pisaster was the undisputed king—which Paine was about to dethrone.

  Each month with the low tide, Paine would, as he put it, “waltz on down to the sacred ground,” count the number of starfish on the experimental side, pry them off, and heave them as far as he could into the surf.

  “From then on,” said Paine, “it was an arms race between me and Pisaster.”

  It was not always clear who was winning. Every month, Pisaster would march back from the depths and reappear on the rock, terrorizing mussels and barnacles like a pack of wild dogs after cats up a tree. And Paine would heave, and heave again. There was a lot of starfish, and a lot of heaving. Paine’s pitching arm suffered rotator cuff injuries. After a couple of days’ battle with the rough skin of Pisaster, the skin on Paine’s hands would begin to peel.

  The longer Paine persevered to throw Pisaster from the rock, the more the rock’s assemblage changed. It began with the acorn barnacles spreading beyond their old bounds. Room for other species soon fell short. Chitons and limpets and some of the algae species decamped. By September the barnacles had covered three quarters of the available space. By the following June, it was the barnacles’ turn to be evicted.

  Without Pisaster to police the grounds, Mytilus was now seriously flexing its muscles. It emerged as the fiercest competitor on the block. It swarmed down, staking out lots with its byssal threads. The rock grew black under a spreading pavement of mussel shells. Paine took inventory. Seven of the fifteen species at the start of the experiment were gone, and all the rest but Mytilus were fast heading for the exits.

  Paine could plainly see where things were heading. After just a year, he had enough on record to share with the scientific world. He wrote it up, his resulting paper appearing in the January-February 1966 issue of the American Naturalist, under the title “Food Web Complexity and Species Diversity.” His hypothesis was stated with this sentence: “Local species diversity is directly related to the efficiency with which predators prevent the monopolization of the major environmental requisites by one species.”

  In other words, the suggestions of Elton, the test tubes of Gause, the theorizations of HSS, now had the cachet of experimental backing in the field. Species indeed were highly interconnected by a web of interactions, a web made more
stable by a complexity of species, a web over which predators could wield inordinate powers.

  Paine’s own interpretation was at turns dutifully restrained and subtly intrepid. He noted both the inherent limitations and sweeping possibilities of this tiny point of rock on an obscure outpost of Pacific shore. “This hypothesis offered herein applies to local diversity patterns of rocky intertidal marine organisms,” he wrote, “though it conceivably has wider applications.”

  Those wider applications would turn Robert T. Paine’s “dumbest” little experiment into one of the most cited papers in the history of ecology. Solid in its simplicity, Paine’s heroic portrayal of Pisaster had laid siege to the stigma that ecological webs were beyond the realm of experimental science. And if one took the serious effort to look, they could very well find predators pulling critical strings in that web.

  In a follow-up paper for the American Naturalist, unassumingly titled “A Note on Trophic Complexity and Community Stability,” Paine coined a term for species of Pisaster’s importance—species whose impact far overcompensated for their relative scarcity. Such species were hereby “keystone species,” wrote Paine. Remove them from the archway of life, and the whole structure comes crashing down. With that, community ecology added a powerful new concept to its lexicon, embodied in Paine’s shining new star.

  Paine and Pisaster spawned a world of new research questions. Which predators matter, which ones do not? What about the deep sea, or for that matter the terrestrial realm? Any keystone predators out there? That is, just how common was such a predator of Pisaster’s impact?

  Somewhere along this line of inquiry came a more anxious slant on the question. A new generation of ecologists freshly weaned on the weekly wonders of Wild Kingdom and the ominous horizons of Rachel Carson’s Silent Spring—presensitized as they were to the specter of mass extinction and the cause of conservation—were reading Paine’s results with a more concerned eye. They were wondering about such predators as wolves and killer whales, great cats and great white sharks. Pisaster had proved that certain predators, by their mere presence, could bolster the diversity of life. But just as easily, once removed, that benevolent hand could be replaced by a phantom fist, knocking species off the planetary rock, as it were, overhauling the living landscape to simpler, cruder states. To these ecologists, the monoculture of mussels crowding Paine’s predator-free rock was handwriting on the wall. It raised the larger question, How are all those big, fearsome, topmost predators doing, anyway?

 

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