An Oasis in the Desert

“What makes the desert beautiful,” said the little prince, “is that somewhere it hides a well.”

—Antoine de Saint-Exupéry, The Little Prince

The sea can be a lonely place, featureless, and nearly devoid of life. Ask those pitiable sailors shipwrecked by Moby Dick and tormented by famine in the central Pacific; ask whale sharks who journey thousands of miles to find a robust meal of plankton. Far from tropical shores, equatorial waters can be pretty as a postcard but deadly as a dustbowl. Their transparency is at once beautiful and menacing, a measure of just how little nourishment can be found. Yet a few outposts of richness dot this expansive, watery desert. Here and there, tiny islands rise to the surface, ornamented by palm trees and surrounded by a narrow fringe bursting with life. Despite the desperately poor water all around them, coral reefs are among the most diverse and productive ecosystems on the planet. Only tropical rainforests, growing on soils similarly bereft of nutrients, boast more species. How do coral reefs muster the abundance, diversity, and productivity that attract snorkelers and divers from around the globe, when the surrounding seas can be virtually devoid of life? What magic trick have reefs summoned to solve the puzzle? The secret is held by some of the smallest animals, and the voodoo potion they have concocted is a mix of alchemy and sorcery that blends a secret supply of energy and the ability to travel in time.

Early naturalists noted that corals grow only in very shallow water. Below about 180 feet, coral reefs give way to rocky bottoms they cannot colonize. Their preference for the shallows reveals part of the magic trick: corals have the photosynthetic capacity to turn light and carbon into sugar, and therefore structure. This life-sustaining alchemy arose on Earth some 3.5 billion years ago, in primitive algae known as cyanobacteria. Modern relatives of those cyanobacteria form a mutualism with today’s corals, cohabitating within the coral’s soft polyps. A coral polyp resembles a tiny vase, with tentacles instead of flowers stretching into the water to capture nutrient particles. But each tentacle also hosts algae, whose photosynthesis helps feed the polyp as it procures calcium from the sea. The base of each polyp in the colony secretes a skeleton of calcium carbonate (a key ingredient of cement) that builds over time into great spires and parapets and atoll-fringing reefs. Without the symbiotic algae the coral would have to subsist only on nutrients floating in the water, which provide a meager diet indeed.

There is one group of animals, albeit very humble ones, that can survive on that lean diet. Simplest of all marine animals, sponges are colonies of cells working in coordination to pump vast amounts of water through hundreds of tiny pores. In a single day, a hard-working sponge can process as much as 40,000 times its own volume in water. Along the way, filter cells lining the sponge’s internal plumbing harvest nutrients suspended in the water. Dramatic forms emerge, as colonies build themselves into barrels the size of a bear, cylinders like a pipe organ, and undulating sheets like parade bunting. Their growth occurs at a glacial pace, but sponges can live for many years, steadily gathering nutrients all the while. The sponge you see today is a time traveler, having compressed years of painstaking construction into a towering and majestic organism, like a time-lapse film of a skyscraper’s construction.

While a sponge is pumping water and sieving it for dissolved organic matter, it continually jettisons filter-specialist cells that have reached the end of their shelf life. Organic matter, sparse in the ocean, is concentrated into sponge detritus and dumped onto the reef where hungry denizens descend on the tasty tidbits. Called the sponge loop, this process of accumulation and repackaging of nutrients delivers a previously invisible source of food to reef communities.¹ Like corals, some sponges also enjoy an energy subsidy from photosynthetic algae that take up residence in their outermost tissues. There is even a direct link between corals and the sponge loop: some sponges gather mucus produced by corals, rich in carbon and nitrogen, and later release more than a third of it to the reef as loose food particles.²

A reef’s complex food web, the feeding interactions of all its members, is laced between the foundation of corals and sponges and algae. A healthy reef is a dynamic and shifting patchwork of algal meadows, boulder fields of hard corals, the fingers and fans of soft corals, massive sponges, and hundreds of other cohabitating species. But like narcissists on stage, these actors all compete for space. Algae are held in check by herbivorous grazers, from damselfishes and surgeonfishes to limpets and sea urchins, who hungrily browse on the rich pasture and keep it from overgrowing the corals. Branching corals with ungulate-inspired names like elkhorn and staghorn grow upward toward brighter sunlight but suffer most when battered by waves and storms. Mound-shaped colonies such as brain coral and boulder star coral are better protected from the ocean’s assault but get overtopped and shaded by their faster-growing competitors. Sponges employ chemical weaponry to attack and usurp mound corals, but they too can be engulfed by the creeping carpet of algae if there are too many nutrients in the water, or too few grazers to manage the mowing.³

While the pillars and slabs of the reef’s foundation are fighting among themselves, they are also sustaining scores of species of fishes, each of whom tilts the battle this way and that. Hard corals feed parrotfishes, who take noisy bites with beak-like teeth adapted to crush the calcium-hardened skeleton and extract the nutritive polyps. Sponges, seemingly soft from the outside, are themselves defended against predation by glass-like spicules and a variety of toxins in their tissues. Nevertheless, angelfishes specialize on sponges, feasting on a smorgasbord of species to avoid overexposure to the particular defenses of each sponge type.⁴ Diminutive bottom-dwellers like blennies and gobies gorge themselves on the detritus continually shed by sponges, and they themselves provide prey to the rest of the food web. And a host of fishes, from massive manta rays to tiny cardinalfish, feast on plankton that gushes from the reef, including clouds of eggs and larvae launched hopefully into the blue sea.

Should any of these fishes be surprised by a rapacious snapper or barracuda, they have but to spring into the cracks, crevices, and holes that abound on a coral reef. To better their odds, most reef fishes live in compact territories they know well, with safe hideouts just a tail flick away. The intricate structure of a reef provides food as well, because the walls and pillars are lined with barnacles, mussels, tube worms, and anemones, sessile animals that use the pillars and pedestals to hoist themselves into rich currents of edible plankton. Once they have colonized a spot, however, they are stuck in place like statues and are fair game for dozens of reef fishes. Wrasses, butterflyfishes, triggerfishes, and many more scour the crenellated surfaces of the reef, probing holes and slipping into fissures to pluck the invertebrates from their plinths.

Reef fishes can effectively exploit the crevices and cracks and candelabras of their undersea cafeteria because they are compact, compressed from side-to-side like a pancake on end, and because they can manipulate their body position with incredible precision. No tuna, as agile as they are in open water, can stand on its head, hover an inch above a rock, then roll onto its side. But angelfishes, tangs, butterflyfishes, and more perform this circus trick all the time. Like gymnasts in slow motion, reef fishes leisurely advance and retreat, pivot and spin; they can even swim backward. Rivaling a NASA spacecraft in their degree of control, they effortlessly adjust pitch and yaw and roll with precise rippling and fanning of fins. Fish are not floating in zero-G, though; their gymnastics are performed in an ocean where gravity pulls at them inexorably. But thanks to a unique organ, they have conquered this pull and maintain perfect neutral buoyancy. This organ set the stage for a sprawling diversity of shapes, fins, and behaviors that gave fishes an all-access pass to the backstage crannies of a reef.

A few million years after sharks and rays branched from the fish family tree, a few primitive mouth-breathers evolved. Mostly denizens of estuaries, those fishes could gulp air and absorb a little oxygen into dense networks of blood vessels in their mouth. Later, out-pocketings of the throat and gut developed, permitting longer air storage and more surface area for gas exchange. And a little over 100 million years ago, a remarkable invention emerged: the swim bladder. This self-contained pouch deep inside the fish can be inflated or deflated like a balloon and provides enough buoyancy to counteract the grasp of gravity. Fishes with swim bladders are perfectly neutrally buoyant, no matter the depth, and their fins are no longer conscripted into a continuous fight to stay off the bottom. Early fishes (and a few still living today) filled the swim bladder by swallowing air at the surface and emptied it by belching. But modern fishes took one more evolutionary stride and invented a sophisticated pump known, inelegantly, as the gas gland.

In advanced fishes, the swim bladder is inflated using dissolved gases in the bloodstream; no gulping and belching for them. The gland itself encases a rich bed of capillaries adhered to the side of the bladder. Inside the gland, a remarkable feat of blood chemistry occurs, relying on the Bohr effect. Christian Bohr studied human physiology in the late 1800s and discovered that when blood becomes more acidic, its hemoglobin has less affinity for oxygen. He also discovered the best way to get a Nobel prize into your house is to raise a brilliant son and grandson, Niels and Aage (both physicists), who each won the coveted medal. Inside the gas gland, the Bohr effect creates a tiny pump. Glucose is converted into lactic acid within the capillaries, and the acidity forces hemoglobin to dump oxygen.⁵ The only place for the gas to go is into the bladder, and voilà, the gland pumps up the pouch.⁶ To shrink the bladder, the lactic acid is withdrawn from the capillaries, boosting hemoglobin affinity and sucking oxygen back into the bloodstream. Molecular evidence reveals that key elements of this ingenious gas-release system first evolved in fish eyes, where rapid delivery of oxygen helps retinas process images faster, the better to see prey and predators.⁷ Later, the same system is repurposed to inflating the swim bladder, an evolutionary leap that unlocks an explosion of reef fish diversity.

Paroled by their swim bladders from the law of gravity, the evolution of reef fishes was unfenced by the need to swim ceaselessly in open waters. Natural selection explored a cornucopia of bizarre shapes, like wafer-thin butterflyfish, tubular trumpetfish, and lovably lumpy frogfish. Freedom from relentless swimming also heralded the emergence of peculiar behaviors, brilliant colors, and novel lifestyles, each a response to the ecological opportunities and physical structures provided by the reef. That oasis of productivity, paired with possibilities bursting from newfound evolutionary elasticity, has yielded a community brimming with creatures so gorgeous and diverse as to rival any ecosystem on our planet.

Seaweed Salad

A person who is growing a garden, if he is growing it organically, is improving a piece of the world.

—Wendell Berry, From a Continuous Harmony

On dry land, whether in the Amazon rainforest or on the sunbaked plains of the Serengeti, life begins with plants. Small herbivores such as mice or rabbits eat tender green leaves and juicy fruits but become targets for carnivores one link up the food chain. Those carnivores—foxes and weasels and their ilk—are also prey for larger, faster, and more ferocious predators. Under the waves, the role of plants is played by algae and seagrass (though only the latter is a true plant). This aquatic greenery is the foundation of the food chain, its anchor link. Nibbling on this foundation are a guild of grazing fishes, small to medium-sized vegetarians who themselves are targets of sea basses and jacks and other predators. Like rabbits feeding foxes, they represent a critical link between the reef’s primary productivity below and the predators above.

Crescent-tailed surgeonfish, brilliantly marked tangs, and vigilant damselfish are among the grazers who frequent shallow, sunlit reefs where algae thrive. Reef vegetarians resemble one another, with characteristically compressed bodies and pointed snouts, lips pursed as if to deliver a kiss. Their fins are broad and blunt, like ping-pong paddles next to a tuna’s long scimitars, and set further forward. This arrangement gives them ultra-precise control over their movements and body position, permitting them to meticulously inspect and pluck the tastiest pieces of algae from the intricate jigsaw puzzle that is a coral reef. Incisor-like teeth are adapted to clip the algae, which is passed to a muscular throat studded with mounds of enamel and dentine: these pharyngeal teeth grind tough algae like a pepper mill. Once swallowed, acids and enzymes break down the algae’s complex polysaccharides, but the fish also gets a little help from some tiny, and not-so-tiny, friends.

Much like cows, which rely on bacteria and protozoans in their gut to digest grass, grazing fishes host a diverse microbial community that specializes in breaking down algal cells. These microbes produce enzymes that chop up the algae’s toughest compounds, which the fish could not digest on its own. Without the microbes, each bite would yield far fewer nutrients, and the fish would starve like a cow pastured on a parking lot. Researchers found something extraordinary, however, when studying bacterial digestion in surgeonfishes (named for scalpel-like spines that protrude defensively from their tails). The fishes all harbor a highly diverse microbial community, but each is dominated by a clan of titanic bacteria 1000 times larger than the others.⁸ Known as Epulopiscium, these mega-microbes would be visible to the naked eye were they not living deep within the fishes’ intestines. There, they churn out digestive enzymes matched to the diet of each fish: bluespine unicornfish (Naso unicornis), named for the fleshy spike poking from their foreheads, favor brown algae and harbor one species of Epulopiscium, while sohal surgeonfish (Acanthurus sohal) teem with a different species better-suited to its preferred red algae. The mega-bacteria even adopt their hosts’ daily schedules, ramping up enzyme production early in the morning, then shutting down the enzyme assembly line as night begins to fall.

Surgeonfishes, who can reach forty years of age if predators are evaded, follow a pattern typical of reef grazers.⁹ They spend their nights in tight crevices, their compressed bodies allowing them to squeeze into the narrowest of sanctuaries. As the sun rises, they emerge to browse on delectable turfs of algae, meticulously maneuvering their snouts to clip preferred flavors. Many surgeonfishes defend algal territories, and smaller species even pair up to guard a patch against larger competitors.¹⁰ They know their territories well, having mapped the best hiding places, shortcut tunnels, and algae-rich plateaus, but will occasionally switch territories, perhaps in search of greener pastures of algae.¹¹

Algae, more commonly known as seaweed, may not be particularly fond of their role as food for grazers. They gird their fronds with biochemical armor that makes their tissues unpalatable or downright toxic. Some are simply mechanical defenses, like calcium carbonate, which renders coralline and encrusting algae nearly as rigid as cement. Other chemicals have more potent effects, interfering with digestion or even working as a poison. Red tide is the most well-known example, an infamous algal bloom provoked by overabundant nutrients—often from agricultural run-off—and excessively warm waters. Staining the sea surface a characteristic brick-red, the algae release toxins that can trigger fish die-offs, shellfish poisoning, brain damage in sea lions, and severe illness in people who eat affected seafood, or even simply inhale the fumes of algal blooms tossed in nearshore waves.¹² The inspiration for Alfred Hitchcock’s film The Birds was a true story about California seagulls disoriented by red tide toxins in their fishy diet that dive-bombed homes in Monterey Bay; driven psycho, they notoriously hurled themselves at rear windows in a frenzy of vertigo.¹³

Back to the surgeonfishes, captive trials revealed they turn up their snouts at unpalatable and dangerous seaweed, and concentrate on the most delectable and least-well defended varieties.¹⁴ From a buffet of fifty seaweed varieties, surgeonfish selected only ten for lunch: none of the favored algae were calcified and none produced toxins, while nearly all species with robust chemical defenses were left untouched. Other scientists working in the Red Sea discovered that seaweed preferences shift as the calendar unfolds. Favoring red and brown algae for much of the year, surgeonfish switched to green algae in the winter, apparently to fatten up prior to the spring and summer mating season.¹⁵ And who could be better qualified to study the reproduction of surgeonfishes than lead researcher Dr. Lev Fishelson?

If grazers choose from their menu of seaweed based on palatability, then a simple solution emerges. Instead of foraging in the wild, plucking what one can find and warily avoiding toxic fronds, why not cultivate your favored food crops on a well-tended field? That very approach has been adopted by damselfishes, the farmers of the coral reef, and it has been so successful that the group has diversified into more than 400 species around the world.¹⁶ It seems that the farming life, in tropical seas, can be a mighty fine life.

Damselfishes are compact creatures, moderately compressed but giving a robust and muscular impression when seen next to a slender and delicate butterflyfish. A bantamweight boxer, with eyes slightly bugged and nose blunted, scowling at the ballerinas drifting lightly by. In adults, the markings are unremarkable: dull browns and blacks, in some species embellished with yellow on the tail or fin tips, or turquoise speckles along the back. Juvenile damsels, in contrast, can be among the most brilliantly painted compositions in the galleries of any reef. Decked out in blazing orange or searing yellow, washed with contrasting azure, ornamented with sparkling cobalt or adorned with peacock-like spots, their flamboyant colors may advertise to pugnacious farmers that they are not a threat to steal from the homestead. More often than not, eye-popping childhood colorations account for adult names: Neon, Sulphur, Azure, Golden, Yellowtail, and Black-and-gold are just a few dazzling damselfish monikers. Sadly, in all species the youthful flamboyance fades as youngsters adopt the business-like dress of their parents.

Adult damselfishes vigorously defend agricultural estates, rocky outcrops with good sunlight and firm substrate on which they find a patch of algae growing. They diligently tend the patch, encouraging the growth of seaweeds they find delicious and nutritious. Depending on where the farm is located—warmly sunlit reef flat, boisterously wavy reef crest, or the cool and dim reef slope—the ideal crop selection will vary.¹⁷ But the end result is a diverse crop of delectable greens surrounded by fallow, rocky tracts dominated by just a few tough and nearly inedible species.¹⁸ Much work goes into tending the homestead. Undesirable species of algae with too many defensive compounds are ripped out. Drifts of sediment are cleared by energetic fanning with their fins. Small pebbles are grasped with strong teeth and dragged to the border. The resulting lustrous algal meadows attract admirers, some of whom come to plunder but others that actually benefit the damsels.

Tender and leafy fronds invite tiny and even microscopic organisms to colonize the rows; like bacon bits, they are eaten with the salad of seaweed, adding protein to the meal.¹⁹ Some farmers have added shepherding to their résumé, by domesticating tiny mysid shrimp whose excrement fertilizes the farm like so many cow patties: damsels with shrimp flocks have richer fields of algae and are healthier thanks to the fertilized produce.²⁰ Though the majority of damsels source most of their food from the farm, recent research using stable isotope techniques (described in the previous chapter) has revealed they select items from a broader take-out menu. Nearly all species will opportunistically grab tiny crustaceans or mollusk larvae swaying in the waters around the farm; for a few species, these pelagic prey make up a whopping three-quarters of their diet.²¹ It appears that some farmers have given up the vegetarian lifestyle, pulled back to carnivory by the savory delights of meat.

A school of yellowtail surgeonfish (Prionurus punctatus) meandering across a coral reef cannot help but be drawn to the appealing greenery of a well-tended damselfish farm. Amid all the stiff, unpalatable, and downright inedible algae the soft and nutritious fronds must be irresistible. And resist they do not. Swooping onto the field like a gluttonous flock of crows (a murder of crows, if you prefer) drawn to fresh seedlings, they descend on the poor damsel’s farm. As the lead intruder approaches, the farmer charges. Though only half the weight of his rival, this damsel is pugnacious by nature, and skilled in the art of defense. He feints an uppercut, then lands a blow. A thumping jab of his snout staggers the surgeon, who turns aside. But another takes its place, and another. Soon, the damsel is overwhelmed and must retreat as the shoal descends. Surgeons clip and gnaw at his precious algae, ravaging his field until they deign to depart, leaving the farmer to assess the damage. Perhaps one day damsels will invent the undersea equivalent of a scarecrow.

Other trespassers include close relatives like the Achilles tang (Acanthurus achilles), a fiery orange spot marking its heel (actually the tail base), who rove in farm-raiding packs. Sea urchins, who lumber onto the fields like implacable porcupines, would utterly denude his farm if not ushered off: damselfishes will seize a spine in their teeth and bodily drag any urchin until it falls off the plateau. But there are others who slink onto the farm, and they come not for the crops but for the landowner himself, including one wolf who dons farmer’s clothing. Brown dottybacks (Pseudochromis fuscus) are elongate fish, shaped like bratwurst, and not much larger than the damselfish they stalk. Like many reef fishes, they come in a few different color morphs—in northeast Australia, a dusky brown or saffron yellow—and can change between them. In the same area, there are yellow and brown species of damselfish. When the dottyback spends a couple weeks around a damsel’s homestead, it gradually adopts the color of the landowner, until it is disguised perhaps as a jolly neighbor coming over for a cup of sugar. Before the murderer can be unmasked, it pounces: the damsel is taken by surprise, overpowered, and eaten. Dottybacks who mimic their prey’s coloration are three times more likely to consummate the kill, a triumph for their mastery of masquerade, but a distressing state of affairs for a damsel.²²

Fish of a Feather Flap Together

It is tough to survive on salad alone. Other than damsels who cultivate a carefully selected menu of nutritious seaweeds, most grazers augment their diet with plankton, detritus, and a host of tiny organisms—crustaceans, worms, mollusks—that live amidst the algae and are swallowed with every mouthful. Some 30 million years ago, however, a suite of adaptations appeared in a few of those grazing fishes that allowed them to gnaw a chunk of coral, crush the cement exoskeleton, and feast on the tender contents.²³ It was like taking a bite from a cinder block and finding candy inside. With every bite, a distinctive crunching sound boomed across the reef: the coral’s defense had been breached. Gaining access to this piñata of soft and nourishing polyps was like a starter’s pistol, setting in motion the diversification of some of the most numerous and flamboyant creatures on any reef.

Parrotfishes earned their name because they swim by flapping pectoral fins like a bird’s wings, and because their large front teeth are fused together into a decidedly beak-like shape. It also helps that most species are brilliantly colorful, dominated by tropical hues of green and blue, and dazzlingly marked with stripes and splashes of red and yellow. Names of many species sound like a 1960s festival roll-call: would the parents of Rainbow, Tricolour, Festive, and Azure please report to the stage? But the oversized, white, and slightly comical buck teeth are what first grab your attention. These represent an incredible feat of evolution, as they are enameled with one of the hardest biological substances on planet Earth.

Pupa Gilbert, a biophysicist at the University of Wisconsin, has investigated animal teeth for years. “Parrotfish teeth are the coolest bio-minerals of all. They are the stiffest, among the hardest, and the most resistant to fracture and to abrasion ever measured.”²⁴ Tiny crystals of fluorapatite are woven into bundles, like medieval chain mail, with bundles getting smaller and harder toward the tip of each tooth. Parrotfish wield these (literally) ground-breaking teeth like chisels into coral, permitting them to eat what no other fish can chew. Dr. Gilbert and her team also studied sea urchins, those spiny invaders of damselfish farms, that gnaw at algae using their own innovative teeth. Each urchin tooth is constructed of offset layers, like a deck of cards fanned for a magic trick, each layer composed of rock-hard polycrystals of calcium and as thin as a scalpel. As the tooth tip is worn down, the topmost layer is shed, exposing the next razor-sharp card in the deck.²⁵ Applied to home cutlery, this advance could put a self-sharpening knife in every kitchen drawer. “The sky’s the limit at this point,” enthuses Gilbert.

Once a parrotfish has bitten a chunk of coral with its formidable teeth, it passes the cement to a specialized grinder in its throat, a separate chewing apparatus known as the pharyngeal mill. These “throat jaws” are set deep within the mouth of the fish, chewing swallowed food even while the front teeth are taking another bite. The mill evolved in parrotfishes (and their cousins, the wrasses) a few million years before the famous fused teeth and was the key adaptation that kicked off their explosive diversification. It is made up of grinding, molar-like teeth attached to a complex set of bones, themselves derived from repurposed gill arches, and a muscular sling that saws the teeth back and forth. Chewing heartily, the pharyngeal mill pulverizes the exoskeleton of coral into a slurry of ground cement mixed with polyps, algae, and all manner of micro-animals living atop the coral. Parrotfishes have no true stomach, instead passing this slurry directly to their intestines, which extract the copious nutrients.²⁶ Combined, the teeth and mill allow parrotfishes to eat what no other fishes can, unlocking access to an immensely abundant food source on the reef.

In a single year, reef parrotfishes are estimated to consume more than 5000 pounds of coral cement per acre.²⁷ All that food has to end up somewhere, as the intestine is a one-way trip, and like a goat browsing on fine fodder, parrotfish release excrement continuously. Parrotfish feces are clouds of almost pure sand, the milled remnants of the calcium-rich coral skeleton. So abundant is parrotfish guano that it forms the principal component of nearly all the blazingly white beaches of the tropics. Something to ponder the next time you are luxuriating on the shores of Fiji: you are rolling and lounging in parrotfish compost.

Because coral is abundant and parrotfishes face little competition while eating it, they can feed themselves with ease, leaving time in the rest of the day to attend to other affairs. Such as affairs of the heart, and the gonads. As in many animal species that enjoy an abundant food source, parrotfish form polygynous mating systems: females greatly outnumber males and choose the largest and fittest male with whom to mate. The same system arises in birds like manakins, who engage in elaborate dances punctuated by wing snapping, and in bowerbirds whose males entice females with elaborately constructed display courts replete with romantic archway. In parrotfishes, the females select males who are brightly colored, which reflects the quality of their diet, and who are swift and vigorous swimmers. As in peacocks, favored characteristics can become extravagantly enhanced, and parrotfishes today are among the most brilliantly colorful species on any reef. Sexual selection within parrotfish arose around 10 million years ago, and the groups in which it dominates (Scarus and Chlorurus) have shown the most rapid diversification since. Of the nearly 100 recognized species of parrotfishes, more than half are in those groups with female choice.²⁸

Polygynous mating systems, known colloquially as harems, have been the subject of intense study, both behavioral and genetic. In birds, males are flamboyantly colored while females are drab, the better to camouflage the nest. The same is true in parrotfishes, where most females are pale or dark reddish or striped; however, there is an added twist. In parrotfishes and closely related wrasses, every single male was born female. These fishes are known as serial hermaphrodites: they emerge from eggs with the capability to express either gender, and to produce either eggs or sperm, but they begin life in a female phase (known as “initial”) and later, if the chance arises, transmogrify into a male phase (“terminal”).

To understand why this happens, consider the sex life of a stoplight parrotfish (Sparisoma viridae). Initial phase adults are modest in size, perhaps a foot long, with a bright crimson belly and the rest of the body checkered with a regular pattern of pale greenish blotches. Nearly all are females (though a tiny fraction are already males, bearing functional testes). Far less common are the terminal phase males, brilliantly painted in a seafoam green, their heads decorated with three stripes of orange-pink, their gill covers and tails adorned with bursts of yellow. Each male dominates a large territory, within which a dozen or more initial phase stoplights may reside. Terminal males initiate a courtship dance involving short bursts of speed, quartering turns, and lunges toward the surface. Disco moves are paired with distinctive popping calls, bursts of sound pulses that entice females and menace rival males.²⁹ The syncopated song-and-dance invites females to join the male in an upward surge above the reef, where eggs and milt (fish sperm) are released in a choreographed cloud. Occasionally, an initial phase male will sneak into the dance and release his own milt, a sly maneuver known to scientists as streaking (and charmingly called bedswerving in ye olde English). Fertilized eggs are then swept from the reef by currents, and juveniles hatch in deeper waters where, hopefully, fewer planktivores are to be found.

From a genetic standpoint, the male’s DNA will appear in every offspring—setting aside the contribution of an occasional streaker—while each female’s genes will be passed on only to her own eggs. Evolutionarily, there is a great advantage in being the terminal male. But what happens when that gloriously colorful male is eaten by a hungry shark? His disappearance will incite the initial stoplights into a frenetic race, physical and hormonal, to become the next terminal male. The female who succeeds in replacing him will seize his evolutionary advantage and dominate the harem’s gene pool. To win the race, initial stoplights ramp up their levels of blood testosterone as estrogen levels decline.³⁰ Initials gradually assume male-like characteristics, including an enlarged forehead and greater body weight. If they outgrow and outduel the other proto-males, they ascend the throne of dominance. Soon they are draped in the colors of a mature male, a process itself triggered by soaring keto-testosterone levels.³¹ Pretenders to the throne, those who fail to surpass the competition, will be evicted from the harem by ruthless attacks from the dominant male. Such bachelor males would find no eggs to fertilize, unless their bedswerving skills were particularly acute, and almost none of their DNA would make it into the future. Thus, most of the contenders revert to the female phase and remain members of the harem where they gradually but steadily toss eggs into the lottery of evolution, biding their time for another shot at the throne.

After a long and exhausting day of courtship, mating, feeding, and streaking, stoplight parrotfish knock off for the night. When evening falls, the risk of being nabbed by a predator soars, so they take a few precautions. Parrotfishes may lounge beneath a coral ledge, or tuck themselves into a cave, or simply recline against a rock on the bottom. But wherever they sleep, they are protected by a unique cloak of invisibility. Special glands in their skin secrete a clear mucus that forms a sleeping bag, wrapped entirely around them like a bubble. The sleeping bag wards off blood-sucking parasites like a mosquito net.³² But the cloak also prevents keen smelling predators from picking up the parrotfish’s scent, safeguarding them through the long night when sharks and moray eels and snappers emerge to patrol the reef for a meal.³³

Nature Red in Tooth and Claw

I bring to life, I bring to death

—Alfred Tennyson, In Memoriam

Among fishes who frequent coral reefs, the overwhelming majority are predators. Over half of all species specialize on eating other fishes, a diet known as piscivory. Much of the predation occurs at night, when killers like barracuda, many snappers, some groupers, jacks, and others emerge to hunt their finned neighbors. Predatory fishes are the largest in any reef community because they can eat only what fits in their mouth. Unlike sharks, who can thrash and tear chunks from large victims like seals and whales, nearly all piscivores must gulp their prey whole. Some, like snappers and jacks, are built for speed. These are the pursuit predators. Accelerating to the speed of an Olympic sprinter or more (sleek wahoos jog at 20 mph but can surge to 48 mph), pursuit predators will chase down slower fish and devour them, aided by their own pharyngeal teeth that crush bone and flesh as a parrotfish mills coral.³⁴ Other predators adopt a sit-and-wait strategy. These artists of ambush, like groupers and stonefish, are often slow moving, large-bodied, and so sumptuously camouflaged as to bamboozle even the most keen-eyed reef fish. Just after sunrise, you might find a grouper waiting patiently, silently, for an unsuspecting mark to swim too close to her enormous mouth. Throwing her jaws open wide, she inhales an enormous volume of water. The hapless victim is sucked into the gaping maw like driftwood into a whirlpool. Noiselessly, her jaws snap shut, water is expelled from gills, and she swallows her first morsel of the evening.

Barracudas, cylindrical and dead-eyed predators who inspire terror in slow-swimming fishes, and more than a dollop of dread in snorkelers, have a different approach. While most piscivores are restricted to swallowing only those fishes that fit in their mouths, a barracuda’s definition of bite-sized prey is far more broad. When a great barracuda (Sphyraena barracuda) attacks, it rushes its victims at speeds in excess of 40 feet per second and seizes them with stiletto-like front canines.³⁵ But if the prey fish is too large to be swallowed, the barracuda grips it firmly in the corner of the mouth, and bites it repeatedly while violently shaking its head in short back-and-forth strokes. All the force of the barracuda’s muscular body, which can weigh over 100 pounds, is employed in this fearsome thrashing.³⁶ Upper and lower teeth in the rear of the mouth work together like scissors, slicing through flesh and bone until the prey is no longer a fish, but rather one mouthful and a couple of bloody chunks. During the butchering, opportunistic fishes often hang around in hopes of grabbing a chunk, large or small, for themselves. Throughout the day, a great barracuda may swim as far as seven miles in search of a meal and can migrate over longer periods to reefs as distant as sixty miles or more.³⁷

Although many predators must patrol large territories to feed themselves, a few piscivores are more stay-at-home types. Moray eels, a diverse group that hunts mostly by dark of night, are far less mobile than barracudas but are highly successful nonetheless. More than 200 species of these snake-like fish slide and slither through the Swiss cheese caves and tunnels of coral and rocky reefs, for which they are finely evolved. Their skin lacks scales, and evolution has jettisoned nearly all fins: both might otherwise hamper their cave-dwelling habits. Only the dorsal and anal fins remain, fused into a continuous ribbon along the top and bottom of their bodies. Some species snatch small fishes from the water, grasping them in dog-like canine teeth, while others specialize on crustaceans and clams that they chew with broad-topped molars. The piscivorous morays specialize in chasing fishes into their sanctuaries, hurtling down narrow tunnels like a kingsnake after a fleeing mouse. Deep in a moray’s mouth are a second pair of jaws that thrust forward to snap at prey and drag them into its throat, a terrifying sight mimicked years ago to startle moviegoers in the science fiction thriller Alien.

Complex hunting techniques have evolved in these wily predators. Morays have been spotted leaping from the water to seize crabs on the shore,³⁸ and even tying their bodies in knots around large prey before tearing the immobilized victim into bite-sized pieces.³⁹ Amazingly, yellow moray eels (Gymnothorax prasinus) tie as many as five distinct knots, including an overhand bend and a figure eight; such dexterity would qualify them for a merit badge at any summer camp. But the most unique hunting method relies on a partner, the roving coralgrouper (Plectropomus pessuliferus). In Red Sea reefs, these huge groupers ambush smaller fishes, sucking unwary prey into their colossal mouths. Those fishes fortunate enough to escape the vacuum attack flee for the safety of the reef, ducking into the first narrow crack they can find. The grouper, unable to wedge its hefty body into the crevice, remains undeterred and instead enlists some help. It cruises to the resting chamber of a giant moray (Gymnothorax javanicus) and solicits assistance by shaking its head and fluttering its dorsal fin.⁴⁰ Aroused from its slumber, the eel dutifully accompanies the grouper to the unfortunate fish’s hiding place, which the grouper points out by performing a headstand. In slips the eel and gulps the absconding fish whole; should the twice-pursued fish manage to evade this slithery attack and bolt from the crevice, it emerges only to find the grouper hungrily waiting to finish the hunt.

While piscivores are busy snapping up unwary fishes, most nonpiscivorous predators on coral reefs hunt invertebrates. They choose from a diverse menu of crabs, clams, urchins, marine worms, and more, plucked from rocks and corals or unearthed from sand and silt. To access these morsels, invertebrate specialists boast an impressive toolkit of highly evolved forms and behaviors. Copperband butterflyfish (Chelmon rostratus) and others use extended snouts like needle-nosed pliers to reach into cavities inaccessible to other fishes. All butterflyfishes are highly compressed and gorgeously colorful, spectacularly barred with yellow or orange or blue, and occasionally stamped with a false eyespot to dupe a predator into chasing the wrong end. Masters of slow, pivoting acrobatics, they undulate pectorals and curtain-like dorsal and anal fins to maneuver into the precise orientation for feeding. Within the snout, brush-like teeth are specialized to glean coral polyps from their holes and pluck invertebrates clinging tenaciously to hard surfaces.

Triggerfishes and filefishes, some of the most fantastically marked fish on any reef (with names like Picasso triggerfish to prove it), hunt invertebrates in a wholly different manner. A triggerfish will hover in a headstand just inches above the bottom, undulating its long dorsal and anal fins like curtains rippling in front of an open window, its mouth pointing at a promising patch of sand. It sucks in a large gulp of water, takes aim, and blasts a powerful jet straight down. Spurts of water stir up the sand, over and over again, excavating a broad hole. Hidden crabs and sand dollars and mollusks are unearthed, which the triggerfish swoops down to capture. Often a dozen opportunistic freeloaders like wrasses and hogfishes hang close by, waiting to slip in and grab an overlooked morsel. But triggerfishes are uniquely specialized for hard-shelled prey, using teeth and jaw muscles that rival those of a parrotfish for toughness. They will occasionally spit out the mouthful, then snatch it again in their jaws to reposition the clam or crab like shifting a walnut in a nutcracker.⁴¹ After a day of digging in the sandbox, the triggerfish will retire by night to a restful cavern, where it wedges itself safely in place using its namesake trigger. Two stout spines in the front of the dorsal fin can be erected, the first sticking straight up to the cave’s ceiling like a deadbolt, the second (the trigger) locking the first in place: only if the trigger spine is released can the deadbolt be folded down. Pinned securely in place, the triggerfish is almost impossible to drag from its cave.

Closely related, and resembling triggerfishes in their oddly rhomboid silhouette and forward-jutting mouth, are the filefishes. These large-bodied reef fish also feed on hard-shelled invertebrates, though they prefer to pluck prey from rocks and corals rather than use the sandblasting technique. Like triggerfish, filefishes swim with symmetrical undulations of their anal and dorsal fins, a highly efficient way of moving their large and heavy bodies through the water, albeit slowly.⁴² They differ in having only a single dorsal fin spine, thus no trigger, and in their unusual scales. Where most fish have smooth and overlapping scales, filefish are cloaked with scales that lie adjacent to one another like bathroom tiles, each tipped with numerous little spikes.⁴³ To the touch, these fishes are rough like sandpaper. Fishermen of yore would keep a dried filefish or two lying about for whenever a rough patch or splinter on their wooden boat needed smoothing. Wielding the dead and hardened fish like an eponymous file, the fisherman swiftly sanded down the offending bit of wood. Today those same spiky scales are being studied by engineers, as their property of encouraging oil droplets to slide only in the head-to-tail direction can be applied to oil pipelines where it would increase efficiency and reduce transport costs.⁴⁴

When not serving as household tools or pipe linings, filefishes show a charming dedication to what can be called parental care. They share these habits with triggerfishes, a complex set of behaviors that distance them from parrotfishes and improve their chances of successfully reproducing. When a male triggerfish or filefish is ready to mate, he prepares a bassinet on the seafloor, a shallow hollow made by blowing jets of water. In some triggerfishes, males and females blow sand together and touch abdomens in a wooing dance ritual. In others, the male may dig the hollow alone, but amid a crowd of males similarly engaged in amorous domesticity.⁴⁵ Resembling a showroom floor of do-it-yourself cribs set out for maternity-curious females, the crowded mating territory is often called a lek. When a female filefish or triggerfish has made her choice, she deposits eggs into the shallow bowl, where they stick fast to sand grains. After fertilization, the male studiously guards the eggs against hungry fishes who would be overjoyed by the prospect of a free caviar lunch.

Fish That Go Grunt in the Night (and Day)

To greet one who is belching or breaking wind is carrying politeness too far.

—Desiderius Erasmus, Collected Works

Karen Maruska listens to fishes for a living. As a marine biologist at Louisiana State University, she spends her days (and a few nights) exploring how and why fishes communicate. Although Jacques Cousteau titled his first book about marine life The Silent World, Dr. Maruska knows the sea is far from silent. “Anyone who’s put their head underwater in the ocean and gone snorkeling, especially on a coral reef, one of the first things you hear is a lot of snapping and popping.”⁴⁶ Her early work was on the diminutive farmers we met earlier. “There’s a lot of species of damselfishes that we now know make sounds. They have a huge diversity in the kinds of sounds they produce and the behavioral context that they use them in.” In her dissertation research, she found male damsels sing an ample repertoire, particularly when enticing females to mate. “There was definitely a sound when he was leading the female back to the nest, that was probably the most characteristic sound, a long series of pulses that kind of sounded like grunts. Males would make shorter pulse trains toward any rival males that were nearby. They also made sounds when they were clearing out the nest … so the female would feel good depositing her eggs there.”

Variations in repertoires can even keep species separate. Bicolor and threespot damselfishes (Stegastes partitus and S. planifrons) live in close proximity, look almost alike, and have very similar courtship displays known as signal jumps. Male rush upward in the water, then dive back down while simultaneously warbling a chirping call. But threespots trill a chirp with three pulses of sound, while bicolors add a crucial fourth pulse. To a discerning female, the difference is like night and day, sparing her the embarrassment of choosing a male of another species.

In well-lit coral reefs, fish rely on their excellent vision to find prey, detect predators, and communicate with neighbors. Bright colors and bold patterns are often found in species like triggerfishes and filefishes who compete over territories and for selection by females. Their virility and fitness are directly on display, since a fish who is a poor hunter or forager cannot engage in vigorous courtship nor match the brilliant colors of better-fed competitors. But as Maruska has found, fish also possess keen ears. Standouts in the chorus of carolers are fishes known as grunts, for the burping rumbles they intone (though the family name, Haemulidae, refers to the blood-red color found inside the mouths of some species). Bearing a close resemblance to their relatives the perches, most family members are nocturnal. Grunts spend their days hanging passively in shaded parts of the reef but venture in groups over open sands once night falls to search for tasty invertebrates. If startled, they will emit a series of their namesake grunts, which sound for all the world like a pigsty full of talkative (albeit aquatic) hogs.

Grunts, and many fishes who use sound to communicate, rely on the swim bladder to amplify their message, like the resonating throat pouch of a frog. In fish, the actual origin of the sound can be quite diverse. Many species have special sonic muscles, attached to the swim bladder wall, which contract and rub the bladder like a balloon.⁴⁷ The result can be a single click, or a sequence of pops, or a drawn-out grunt. This technique is shared by cod and their relatives, who sing in cooler, more temperate waters. Other fishes generate sound with their pectoral fins, which are connected to the body by tightly strung tendons that twang like guitar strings as the fins beat.⁴⁸ Sunfishes, whom we have met before, and clownfishes (those adorable anemone-dwellers made famous in animated films) depend on their pharyngeal teeth to make sound, grinding their molars and amplifying the vibrations with the swim bladder.

In grunts, the vocalizations appear to warn of threats, as first noticed by fishers when the unfortunate grunt was hooked or netted. In others, like damsels and parrotfishes, a variety of sounds are broadcast during courtship. Parrotfish strenuously slap their opercula (the gills’ hatch-covers) like a tambourine. As with color, those fishes who are large and well-fed produce more vigorous calls, so choosy females can use sound quality to estimate the calling male’s fitness. Sea robins, curious creatures who scuttle over the seafloor with spines projecting like crab legs from their dorsal fins, make conspicuous drumming sounds during spawning. This vocal habit was known as far back as Aristotle’s time and was later likened to the tireless crooning of their namesake bird.⁴⁹ As sea robins grow larger, their underwater voice gradually changes from soprano to bass, thus communicating the singer’s size.⁵⁰ Closely related gurnards, who resemble sea robins in using fin spines to comb the seafloor for small crustaceans, vocalize strenuously while competing over food.⁵¹ Like hounds vying for food from a single bowl, a gurnard growls and makes aggressive rushes toward challengers as it circles a feeding site. Once it seizes a crab, the lucky gurnard trumpets a series of intimidating knocking sounds while scampering off with its prize.

Among the diverse undersea chorus, the most expressive vocalists must surely be the toadfishes. They owe their amphibian nickname to their broad heads and wide gaping mouths, and to their tendency to crouch, camouflaged, on sandy or silty bottoms. But mostly for the delightful croaking noises they produce, honks readily audible even to snorkelers. Short pulses resembling burps from a French horn are produced by both sexes, while a longer tone like a boat whistle is tooted by males alone.⁵² This sonorous boat-whistle call is aimed by a swim bladder specially evolved to amplify the sound and focus it forward. Toadfish possess special sonic muscles, attached to the swim bladder, that contract much faster than typical white and red muscle fibers, generating sound frequencies greater than 100 hertz (about two octaves below middle C).⁵³ After building a nest of shells and stones, the male’s song entices females to lay eggs there.⁵⁴ Maruska noted that the nocturnal habits of these fish influence their use of sound. “Toadfish and midshipmen rely heavily on acoustic communication. They do a lot of their spawning at night, so visual cues aren’t really important. They make these really loud, long-duration hums that males make in the nest … trying to attract females. Females will home in on male sounds, and choose a male based on his sounds.”⁵⁵

Unfortunately for toadfishes, tooting your own horn can get you in trouble. Dolphin trouble that is. It turns out that bottlenose dolphins, who sing complex underwater songs of their own and boast exceptionally keen hearing, have learned to home in on toadfish whistling. In the waters off Florida, toadfishes make up an eighth of all fishes eaten by these dolphins, a staggering haul considering each dolphin can polish off more than 12 pounds of fish in a day.⁵⁶ Playback experiments show that dolphins can track their prey by sound alone and distinguish delectable menu items from inedible ones. As the evolutionary war of water words heated up, toadfishes adopted a prudent course of action: shut up while danger is near. When the clicks and pops made by dolphins are audible, toadfish cut their boat-whistling in half (while stress hormones flood their bloodstream) as they cower until the threat has passed.⁵⁷

Neither toadfish nor dolphin can tune in to the other’s song, however, if there is noise blaring in the background. Like a safecracker trying to open a vault, they need silence to hear the fine details. Regrettably, today’s oceans are far more noisy than they were a hundred years ago. World boat traffic increased fourfold in two decades (1992–2012), and all those engines are filling the seas with a loud rumble that threatens to drown out fishy communication.⁵⁸ Motor noises cut in half the distance at which the Lusitanian toadfish (Halobatrachus didactylus) can hear boat-whistle calls from neighbors,⁵⁹ and oyster toadfish (Opsanus tau) are known to call more loudly when boats are near, a wasteful expense of much-needed energy.⁶⁰ In Brazilian damselfishes (Stegastes fuscus), who communicate volubly with underwater pops and clicks, even the noise of people partying on shore can be an annoyance. During the peak days of that country’s famous carnival, roving trucks can pump the sound of samba at well over 100 decibels. As the racket mounts, damsels were observed to abandon grazing more readily, and even overlook predators until they were only inches away.⁶¹ What might be a party for people sounds like a jangling, distressing nuisance for fishes.

We are only just beginning to pull back the curtain and understand the pageantry of coral reefs. Thanks to Karen Maruska, we know more than ever about fish communication, but countless mysteries remain. “I’ve always just been fascinated by fishes and their diversity. And just understanding how they do things, like reproduce. They’re just so weird, and it’s fun. Everything you do is learning something new. As a scientist, that curiosity always gets you up in the morning.”⁶² That same curiosity has inspired millions of people to swim, scuba, and snorkel through coral reefs, appreciating and documenting the diversity they find. That diversity includes fish species, but also their colors, patterns, shapes, sounds, and performances. What they continue to discover is staggering. On the stage set by coral reefs the greatest show in the sea is playing, and the cast of characters includes some of the weirdest, wildest, and most extraordinary creatures the planet has ever seen.