The Four-Eyed Man Is King

Darkness there and nothing more.

Deep into that darkness peering, long I stood there, wondering, fearing

Doubting, dreaming dreams no mortal ever dared to dream before.

—Edgar Allen Poe, “The Raven”

Only a thin layer of the ocean enjoys the kiss of sunlight, as Jacques Piccard saw firsthand. Depending on water clarity, daylight penetrates to only 600 feet or so; faint twilight reigns to about 3000 feet, beneath which the ocean is enfolded in total darkness. Between those two depths the temperature plummets too, the sun’s warmth fading rapidly. From there to the bottom, a thermometer will register just a few degrees above freezing, around 36 °F. In one of the sea’s great contrasts, the sunlit layer is home to approximately nine-tenths of all marine life, and yet comprises a scant 5 percent of the ocean’s volume.¹⁵ Hunters in this thin layer of abundance rely on vision more than any other sense, but at depth this tool is increasingly blunted since light is degraded in myriad ways. As you dive deeper into the sea, sunlight gradually fades to a miniscule fraction of its surface brightness, with just 1 percent of photons penetrating to 1000 feet. Because water does not absorb all parts of the spectrum equally, the quality of the light shifts as well. Midwater colors are skewed: reds are filtered first, then yellow, and soon only shades of greenish-blue remain. Everyone at depth has a case of the blues. And as minute particles in the upper ocean absorb any photons scattering from side to side, soon all the light that reaches deep waters arrives only from directly overhead. Look up, and you can just see a glimmer of the sky, and perhaps a silhouette of a fish or squid; look sideways or down, and all is inky black. The only other light at these depths is bioluminescence emitted by fishes and shrimps and jellies that glow like pale blue fireflies.

In response to the peculiarities of ocean twilight, fishes have developed phenomenally sensitive eyes and evolved downright bizarre solutions for seeing in the near-dark. Most twilight zone fishes have large eyes with enormous pupils to admit more light, like the descriptively named owlfish (Pseudobathylagus milleri), just 6 inches long with an eye nearly an inch across. Fish peering into near-darkness have extraordinarily sensitive retinas, with large light-sensing rods for capturing scarce photons. Because larger rods reduce acuity—the ability to see fine detail—in some fishes the retinas feature discrete areas packed with smaller, tightly grouped rods, like a built-in magnifying glass.¹⁶ All those detectors are tuned to the blue-grey color of downwelling light, though some midwater denizens like dragonfishes add an extra rod type capable of perceiving shortwave radiation that also penetrates the gloom.¹⁷ Silver spinyfin eyes (Diretmus argenteus) possess as many as thirty-eight rod pigment types, compared with just one in terrestrial animals, to better capture the deepwater spectrum.¹⁸ In many midwater fishes, the rods are arranged in layered banks to increase their sensitivity to dim light. In the eyes of escolar (Lepidocybium flavobrunneum), up to six banks are packed onto the retina, yielding an astounding density of 1.5 billion photosensors per square inch (25 times more than today’s most sophisticated digital cameras).¹⁹ Those rods deliver signals to a much smaller number of nerve endings, a phenomenon known as spatial summation that drastically increases the retina’s sensitivity. And if a photon should manage to pass all those rods without being detected, twilight fishes like the escolar and many others possess a tapetum lucidum mirror behind the retina to bounce the strays back for a second viewing.

All these adaptations allow fishes of the twilight to hunt in the dimmest of light. They improve their chances by staring up into downwelling surface rays to catch a glimpse of a prey’s silhouette. The eyes of many midwater fishes are located atop their heads; like perpetual optimists they are forever looking up. One of the most bizarre of these sky-watchers is the barreleye (Macropinna microstoma), a bulbous and slow-moving fish who appears to have a large, smooth forehead and tiny, puckered eyes. On closer inspection, the “eyes” turn out to be nostrils, connected to a finely tuned olfactory system. The true eyes, barrel shaped marvels of engineering, are lodged within the fish’s forehead. No lids betray their presence, and no pupils are externally visible. Instead, these tubular eyes peer through a forehead composed of utterly transparent tissue, like twin telescopes aimed through a glass skylight. Broad light-capturing lenses are permitted by the tubular design, much larger than if the eyes were spherical, and the double-barrel design provides excellent depth perception. They can even shift their eyes, twisting the tubes inside their foreheads until they can see straight ahead.²⁰ This orientation helps them detect predators and also attack their favorite prey, ribbon-like jellyfish relatives known as siphonophores. Looking up, the barreleye can detect a siphonophore’s silhouette, but when it closes in to feed on the tentacles, the forward view helps them pick delicately at their meal to avoid being stung.

Other fishes have tubular and upward-pointing eyes, like the appropriately named telescopefish (Dolichopteryx longipes), but these creatures have solved the problem of forward vision in an entirely different way. Their eyes protrude slightly from the head and are fixed in position, unable to rotate forward. Instead, to detect the faint blue bioluminescence of prey and predators swimming in front of them, telescopefish possess an extra lens on the side of each squat, tubular eye. Light from ahead of the fish passes through this lens, then bounces off an internal mirror to strike a secondary retina draped on the opposite wall: the eye can see above and in front of the fish simultaneously.²¹ Perhaps these marine marvels should instead be called periscopefish. The mirror is unique, composed of stacks of silvery guanine crystals arranged almost like a lens, so the reflection produces a well-focused image. Such eyes were the first ever discovered in vertebrates, an entirely novel visual system that can form images with a mirror.

Fishes that can be seen by predators lurking below them are under powerful pressure to hide their silhouettes. Numerous twilight zone fishes have evolved light-emitting photophores on their belly that glow with a color and intensity matched precisely to the light filtering from overhead, obscuring their outline when viewed from below. Photophore brightness must be dynamic as well. When radiant lanternfishes dive into darker waters they dim their underbelly glow; as they ascend, nerves connecting eyes to photophores increase the brightness, rendering them practically invisible at all depths.²² So widespread is this adaptation that it can be found in more than forty families and hundreds of species of fishes, not to mention crustaceans, squid, jellyfish, and myriad other denizens of dimly lit depths.²³ Remotely operated submersibles conducting deep-sea surveys with highly sensitive cameras found an astounding three-quarters of 350,000 animals displayed bioluminescence (not far from Beebe’s informal estimate).²⁴ In some species, photophores produce light through a chemical reaction nearly identical to fireflies: a protein and an enzyme, devilishly called luciferin and luciferase, combine like the two liquids in a glow stick, and energy is emitted in the form of light. Others rely on symbiotic bacteria to produce the light, and their photophores are adapted as chambers to keep these helpful bacteria alive and aglow.

A special case of bioluminescence gives lantern sharks their radiant nickname. These diminutive deepwater sharks, distant relatives of great whites and hammerheads, are attractively dappled with blue photophores, the proverbial wicks making their namesake lanterns glow. In one family, prosaically dubbed the “dwarf mesopelagic sharks,” photophores are restricted to the belly and their brightness fades around the sides, a phenomenon known as counter-shading or better still, counter-illumination.²⁵ When seen from below against overhead light, the adaptation produces a perfect camouflage for this pelagic, midwater family. A second family of lantern sharks contains mostly demersal, or bottom-swimming species, for whom counter-illumination is unnecessary. Instead, an indigo glow is employed by amorous suiters to signal in the darkness for prospective mates. Photophores are arrayed in complex and species-specific patterns, in patches on the flanks, eyelids, and tail. Receptive partners search the blue light district for a familiar pattern of lights and slide in quietly to make an acquaintance. A couple of these shark species even use lamp light to advertise poisonous spines in their dorsal fins, highlighting them with a few strategically placed glowing spots.²⁶

Unfortunately, illuminated lotharios also attract the attention of hungry predators, lurking wide-eyed in the gloom. In response, many bioluminescent fishes gamble only on intermittent flashes of light, timed to minimize their risk of being eaten but maximize the chance of finding a mate. Researchers assessing fish swimming speeds and mate densities estimate that a cautiously flashing female can find a receptive male in as little as two to four hours, but still these are risky hours, and a cat-and-mouse game of evolution and counter-evolution is underway.²⁷ Predators have harnessed photophores themselves, to shine like a spotlight and illuminate prey, turning their own tricks against them. Not to be outdone, prey developed darker and darker skin: deep-sea fishes are among the blackest animals on the planet, achieved through tiny melanin crystals arranged on their skin so as to side-scatter any incoming light.²⁸ At the very bottom of the ocean, many fishes have red-tinted skin that appears black when struck by blue light, because the skin has nary a particle of blue to reflect the beam. But in a final twist, dragonfishes (Malacosteus) evolved a red “sniper scope” to outwit these rosy-skinned fishes. Beamed from special photophores beneath their eyes, the scope’s red rays are tuned to reflect off the crimson-tinted fishes and light them up as brightly as a drive-in movie screen.²⁹

When light fails to safely attract mates, fishes turn to perfume. Many species, such as the twilight zone–dwelling hatchetfish (Argyropelecus hemigymnus), rely on their sense of smell and release of pheromones to detect and summon partners for reproduction.³⁰ Underwater perfume likely provides the first clue a potential mate is in the neighborhood, as it travels much farther than the dim blue light of photophores.³¹ Hatchetfishes pair exceptionally sensitive noses with their own form of double vision: oversized eyes that bookend severely flattened heads boast complex retinas with twin areas of high sensitivity, one at the bottom for receiving overhead light and one near the back that can view potential mates ahead.³² But when swimming in total darkness, olfaction provides a handy system of distant detection. Abyssal grenadiers, known ingloriously as rat-tails (a reference to tails tapering to a point rather than a terminal fan), find food by scent alone, in utter darkness. Cameras monitoring food baits in the North Pacific, suspended at depths below 19,000 feet, revealed that grenadiers arrived within minutes and began feeding ravenously. Baits were discovered sooner when there was strong current to scatter its odor, with three-quarters of the diners arriving from the down-current direction, clear indication that the hungry fishes were following the tantalizing aroma of dinner.³³

Sometimes it is not dinner that lures diners with a wafting scent. In deep-sea anglerfishes it is the cook herself who entices patrons with a different sort of hunger, reeling them in with an irresistible perfume. Anglerfishes are a taxonomically sprawling group (more than 320 species; bioluminescent courtship yields surprisingly high rates of speciation) composed of squat, lumpy, gargoyle-like fishes equipped with enormous mouths and distensible stomachs, and bristling with a variety of odd appendages.³⁴ Most notable is a unique fishing apparatus composed of a bent rod-shaped stalk (itself derived from the foremost dorsal fin spine) tipped with a lure called an esca. Often bioluminescent, the esca dangles in front of a toothy mouth where it attracts both prey and partner. Anglerfishes live in low density, and their sluggish swimming abilities can make finding a mate difficult. Instead of searching the sea, females release a powerfully appealing pheromone to draw mates to them. Males home in on the scent using their oversized nostrils (reputed to be the largest of any vertebrate), then follow the light of the dangling esca until they latch on to a partner.³⁵ Literally. Males are a mere fraction of the size of an adult female, and when first discovered they were thought to be tiny, external parasites. Which, in truth, they are.

Many anglerfish males have nonfunctional mouthparts and will die if they do not find a mate. Once joined in watery matrimony, the male attaches to the female’s body, dissolves her skin with a salivary enzyme, and connects his circulatory system to hers. Like a leech, he draws nutrients directly from her and will never live a solo existence again. Anglerfish with parasitic males (about half the known species) have immune systems peculiarly adapted to this curious behavior. Unlike people, in whom organ grafts are often rejected with disastrous consequences, these anglers lack the histocompatibility pathways that flag foreign tissues for destruction by T-cells: they literally cannot distinguish between their own flesh and that of their mates.³⁶ Meanwhile, the male’s gonads are stimulated during fusion with the female, and soon he is able to release sperm into the water to fertilize her eggs. In a few species, the female decorates herself with as many as eight males, each contributing to reproduction, albeit to no other chores of domesticity like swimming or foraging.³⁷ One wonders if not a few human females might assess the role of their males as being similarly limited in supportive scope.

Morsels, Tidbits, and Cornucopias

When Piccard peered out of his bathyscaphe as it descended into the darkness, the craft’s exterior lighting illuminated motes of organic matter sinking ever so slowly from the surface. He called those morsels “snow,” a term coined by earlier explorers. Fishes and other animals of the deep sea rely on these particles, as a mouse relies on crumbs brushed from a café table. More trash than snow, the steady drizzle of particles includes dead algae, cast off exoskeletons, deceased copepods, fish scales, and feces from schools foraging in the sunlit shallows. That snow is relentlessly assaulted as it descends, by all manner of organisms from bacteria to zooplankton, shrimps to squid, and countless fishes. Paucity of food means fishes survive only at low densities, far lower than their shallow-water relatives; that deepwater scarcity presents challenges for prospective mates and demands for hungry predators. If you are going to forage in deep, black waters, you are going to need some skills and adaptations, the likes of which almost never arise in fishes of the shallows.

Attracting prey with a simple light, a glimmer they may mistake for a tasty shrimp or other tidbit, is a popular approach. Our lovelorn friends the anglerfishes hang from their foreheads a glowing esca as bait, with forms unique to each species, ranging from a simple blob to fanciful shapes that resemble brushes or the gnarled fingers of a witch’s hand. The lure’s lamplighters are symbiotic bacteria that reside within the esca, their glow echoing off mirror-like guanine crystals that line the esca’s walls.³⁸ Bacterial mutualisms also are harnessed by ponyfishes (Leiognathus), and the fittingly named flashlight fishes (Photoblepharon) who sport bright, forward-facing headlights under each eye.³⁹ Once the bewitched prey is drawn within reach by an anglerfish’s lure, the innocuous-looking owner throws open its enormous mouth like an attic trap door, sucking water and the hapless victim into its gaping maw. The largest mouths in the marine realm belong to deep-sea fishes, sometimes comically dwarfing the diameter of their own bodies, a toothy opening so cavernous they can even swallow a fish larger than themselves.

Among bigmouth fishes the pelican eel (Eurypharynx pelecanoides) is the most surreal, straight from the pen of Salvador Dali. Its ribbon-like body connects to a rounded head that nearly splits in half, like a walnut, when the jaws are unfolded. So unusual is this eel’s architecture that it has inspired new designs in 4D printing, solid structures fabricated in three dimensions that fold into new conformations, like origami, in response to heat or light.⁴⁰ In case the snack is not entirely flushed down the throat by a tidal wave of water, huge dagger-like teeth foil quick getaways, a terrifying adaptation brandished by bristlemouths (an excellent moniker in its own right) as well as anglerfishes. The stomach is distensible to accommodate the recently gulped dinner, a common adaptation among dark-water predators, and it can swell to preposterous proportions, turning the fish into a veritable football with teeth and tail. And because many of the captured prey are bioluminescent themselves, stomachs of most abyssal predators are lined with jet-black pigments. Once a shrimp or fish has been seduced by dreamy light, stabbed or gulped whole, and swilled into the ebony stomach, no light escapes to mark its end nor illuminate the clandestine killer. A few predators go one step further, like the golden sweeper (Parapriacanthus ransonneti), who gobbles up glowing copepods by the hundreds then mobilizes their enzymes to power its own underbelly glow, a light source elaborately titled klepto-protein bioluminescence.⁴¹

If a meal is hard to come by, and starvation is to be avoided, then a fish must expend as few calories as possible. Efficiency is rewarded at great depths: anglerfishes, for example, are models of patience as they float motionless, waiting for prey. Tripodfishes stand on the bottom, perched on three slender stilts formed from pelvic and tail fin spines that lift them above the silty floor to just the height preferred by their favored lunch of shrimp. They are hermaphrodites, capable of mating with whomever happens to stilt-walk by, and thereby conserve energy otherwise spent on chasing down a suitable mate.⁴² Many deep-sea fishes must travel to find food, however, and here evolution has honed locomotion to achieve maximum forward progress with minimum effort. Because dark-water fishes do not rely on visual cues when hunting, there is no chasing of quarry that requires bursts of speed, or quick cornering. Predators instead are languid, biding their time, keeping their metabolism and oxygen consumption low while relying on unhurried swimming until they bump into a prospective prey item (sometimes quite literally).⁴³

Grenadiers, those rat-tailed bloodhounds of the deep, earned their unpleasant epithet for their eel-like tails (decidedly not rat-like) and an undulating swimming style that is the pinnacle of efficiency. Hydrodynamic studies have shown that eel-like swimming can propel its pilot four to six times farther than a typical fish while expending the same amount of energy.⁴⁴ Tails undulating like ribbons are not exclusive to eels and rat-tails; many deep-sea fish have adopted them, including the ancient frilled sharks (though no sharks inhabit the true abyss).⁴⁵ These living fossils gradually lost the lower lobe of their ancestors’ bi-lobed tails until all that remained was a long thin ribbon. Sharks of the deep sea, whether ribbon-tailed or original flavor, also swim more slowly than close relatives who hunt in shallower waters, further conserving meager energy supplies.⁴⁶

All these adaptations—bioluminescent lures, bi-directional eyes, low metabolism, and eel tails—are driven by the extreme scarcity of nutrition in the dark depths of the ocean. But there are a few places at the bottom of the sea where scarcity is but a memory, and a cornucopia of food is freely available to those able to dine at some very peculiar tables: whale carcasses, seamounts, and boiling water volcanoes.

Every few days a whale dies of natural causes, taking its last breath at the surface of the open ocean. Drawn by the inexorable hands of gravity and density, its heavy body soon dips beneath the waves and sinks slowly into the blue-black gloom. Eventually, it comes to rest on the bottom. In days of yore, before the whaling industry brought slaughter to the seas, large whales may have numbered more than 2 million.⁴⁷ Even a conservative estimate of their mortality (around 4 percent annually) suggests that as many as 200 whales may have expired every day and sunk to the bottom.⁴⁸ In a food desert like the deep seabed, the arrival of a single whale’s carcass weighing 40 tons is the equivalent of having a cargo plane full of fried chicken land at your fasting retreat. For animals eking out a famished existence in the deep sea, this cornucopia from above represents the equivalent of two centuries of organic snow, a concentrated banquet for those who can find it.⁴⁹ Across all oceans, whale falls may contribute as much as 9 pounds of food to every acre of the seafloor, every single year.⁵⁰

When a whale hits the bottom, its arrival triggers a scramble of diners. Among the first to gather are sleeper sharks (Somniosus pacificus and relatives), snub-nosed and slow-moving predators that feast on whale falls over the continental shelf.⁵¹ Ravenously they latch on to the giant’s flanks, then furiously spin their bodies to rip loose ragged chunks of flesh. Smaller rat-tails slip between writhing sharks to slice a piece from the cadaver, or scrounge stray morsels scattered by others. Snubnosed eels (Simenchelys parasitica), who often parasitize living fishes by lodging themselves in shark hearts, may be among the most numerous feeders.⁵² Eel-like hagfishes—slimy, jawless relatives of lamprey—burrow into the whale like drills, then eat from the inside out. These early scavengers take 100 pounds of flesh per day from the carcass, for weeks on end. Smaller and smaller fishes, and many invertebrates, nibble their own tidbits until eventually only bones remain. A single great whale may sustain such hordes of scavengers for a year or more before its flesh is stripped clean. Even then, a skeleton chock-full of nutrition remains.

Exposed bones are swarmed by crabs, shrimp-like amphipods, and marine worms, which themselves are snatched up by sharks and other deepwater predators. Years later, when only the hardest and most inedible parts are left, still digestion by the deepwater community continues. A rich assemblage of bacteria relying on sulfur for energy (more about this in a moment) invades the skeletal shards. These microbial colonists slowly break down marrow lipids that account for half the mass of whale bones, a process that can stretch to fifty years until the last vestiges of a great whale finally turn to dust. More than 400 species of fishes and invertebrates rely on whale falls, more than are found on any other patch of ocean floor, and many of which occur nowhere else.⁵³ Some ichthyologists have speculated that shallow-water organisms may have used whale carcasses as stepping stones, guiding them ever deeper into the ocean and permitting the first colonization of the abyssal depths by species formerly restricted to coastal, nutrient-rich waters.⁵⁴

Wherever nutrients accumulate in the ocean, one will find eruptions of fish diversity and abundance. Nowhere is this more true than around seamounts. Rising like desert mesas from the seafloor, these undersea mountains range from narrow ridgelines to massive tables of bedrock. Though they never crest the surface, the local gravity of giant seamounts draws water toward them, pushing up a bump on the sea that can be spotted from space. Satellite altimetry surveys estimate Earth’s oceans may be studded with as many as 100,000 giant seamounts taller than 1000 feet; smaller undersea hillocks and knolls likely number in the tens of millions.⁵⁵ No matter how numerous, each mountain is a nutritional hotspot that can sustain massive fish schools. Seamounts divert prevailing currents to create local upwellings that draw nutrients and much-needed oxygen toward the mountaintops, and block sinking organic snow from falling further into the abyss. They also impede the daily vertical migrations of zooplankton, trapping millions of these tiny animals at the summit during dawn dives.⁵⁶ Peaks and flanks of seamounts are colonized by thickets of cold-water corals and diverse communities of sponges, anemones, crabs and shrimp, sea stars and urchins, squids, sea cucumbers, and marine worms. Midwater grazers and planktivores find ample food supplies on and above these marine monuments, browsing on the rich buffet line of benthic invertebrates or sieving stymied plankton from the water.⁵⁷ Nearly a thousand types of fishes are sustained by this buffet, many completely new to science, and a single site can host hundreds of species and millions of individuals.⁵⁸ Massive shoals of small fishes eddy above seamounts, much more populous than in the open ocean, and their abundance attracts the attention of huge schools of predators who hover nearby.

Perhaps the most famous of these looming predators, celebrated worldwide as a delectable menu item in seafood restaurants, is the orange roughy (Hoplostethus atlanticus). Formerly known to marine biologists as a slimehead, this formerly hyper-abundant fish was subjected to an all-too-effective rebranding campaign when colossal schools were discovered around seamounts off the coast of New Zealand in the late 1970s. There, schools of orange roughy congregate to feast on the prawns and squids and smaller fishes drawn to the bounty of nutrients amassed around these underwater mountains. Like other denizens of deep and cold waters, orange roughy are sluggish, with a slow metabolism and lethargic swimming style. They are some of the oldest fishes in the sea, routinely living beyond 150 years and perhaps even reaching two and a half centuries.⁵⁹ In other words, the fish on your plate could be older than the United States of America. Concomitantly late to reproduce, an orange roughy will not mate until it attains twenty or even forty years of age. All this means that enormous schools of adult orange roughy took an enormous amount of time to reach that abundance. Once fishing began, with trawl nets deployed relentlessly on and around their favored seamounts, populations plummeted and never recovered. Those nets irreparably damage the rich but delicate ecosystems that drape the flanks of ocean mountains, cutting off the legs of the buffet table that supports all that fish life. While recovery is possible, if fishing pressure is firmly controlled, seamounts are too isolated to enjoy rapid recolonization by fishes, and evidence suggests even partial recuperation will take decades or centuries.⁶⁰

It is hard to blame fishing communities, however, for delving into the proverbial pot of orange gold at the end of a watery rainbow. Around a single seamount off Tasmania known as Saint Helen’s Hill, orange roughy catches netted trawlers US$17 million in just three weeks.⁶¹ One net run could haul in 50 tons of fish, thanks to the slimehead’s habit of clustering together as tightly as do cod. For New Zealand, here was a rich new source of revenue, one that in peak years landed 60,000 tons per year and annual revenue in excess of $65 million.⁶² But fish can only be caught sustainably if their reproduction is able to replenish the stock, otherwise you are sacrificing the future by eating up the product of history. And the outlook for orange roughy swiftly turned dim, sacrificed on the barrelhead of local and national financial gains. Just as readily as fish filled nets and dollars filled bank accounts, so too came the rapid decline. In New Zealand catches nosedived after boom years in the mid-1980s, and by 1997—not twenty years after the fishery had opened—orange roughy populations had plummeted by 80 percent.⁶³ On the other side of the world, an orange roughy fishery in Ireland opened in 2001, catches peaked just one year later, and by 2005 the fishery had utterly collapsed.

In contrast with the North Sea’s extremely fecund cod, who may release more than a million eggs in a breeding season, an orange roughy adult normally produces only a twentieth of that lavish output.⁶⁴ Despite the apparent richness of seamounts, the limited reproductive potential of fishes who thrive at these sites, combined with their glacially slow growth to maturity, makes fisheries collapses as seen in Ireland and New Zealand inevitable. Despite the richness of seamounts, those fish simply cannot reproduce quickly enough to offset the arrival of high-tech trawlers, and they have no means to accelerate their procreation. But deeper still, hidden from the eyes and fishing nets of the world, lies another constellation of nutrient hotspots where animal life is unexpectedly abundant. And while seamount fishes have not yet evolved a way to accelerate their reproduction, such advances have been invented by other deepwater species, some of whom discovered an extraordinary use for an abyssal environment so strange that it is quite literally unlike anywhere else on planet Earth.

Freezing Cold, and Boiling under Pressure

Double, double toil and trouble;

Fire burn, and caldron bubble.

—William Shakespeare, Macbeth

On land, the record-holder for longest pregnancy is a female African elephant, who carries her calf for twenty-two months; Asian elephants are close runners-up, with gestations lasting eighteen months or more.⁶⁵ But both trail the pack when marine animals are added: the eggs of some deep-sea fishes require an astonishing four years to develop, more than twice as long as an elephant. One such species is the spiny skate (Bathyraja spinosissima), whose four-horned egg cases—the curious mermaid’s purse that distinguishes skates from rays—can repose on the seafloor for 1300 days or more before a tiny skate emerges. Development is slowed in the coldest waters to as long as 1500 days, a perilous delay that gives egg-eaters several extra months to snatch and devour a forsaken purse. Temperature plays a strong role in the development of many animal eggs, from turtles and alligators (in which gender is determined by egg temperature) to all manner of fishes. But in slow-developing species like the spiny skate, there is severe evolutionary pressure to find warmer locations that can accelerate egg development. The sooner your young emerge, the more likely they, and your species, are to survive. What the skates hit upon several million years ago were not discovered by humans until 1976: underwater volcanoes spewing boiling water.

KC and the Sunshine Band’s “Shake Your Booty” was turning up the heat in discos around the world when a doctoral student named Kathleen Crane went to the Galápagos Islands to investigate deepwater temperature anomalies. Her dissertation supervisor, not optimistic about her chances, advised her to “find another thesis topic … you’ll never find hot springs on the seafloor.”⁶⁶ But on June 2, after more than a month at sea, her determination was rewarded as their sampling device struck thermal pay dirt. “The Deep-Tow swept over warm water emanating from the fissures in the rift valley below. We recorded a temperature increase of 0.1 °C (which was a phenomenal increase given the Deep-Tow’s height above the bottom), and we trapped bottom water in Ray’s bottles. For three days I did not sleep more than two hours … I knew we were on the verge of something momentous.”⁶⁷ Crane and the team had found the world’s first hydrothermal vent.

At the Galápagos site and many discovered since, deep cracks in the Earth’s crust reach down toward molten magma several hundred miles below. Seawater percolating through these fissures is heated, as in the boiler of an apartment building, and steams its way back up to the ocean floor. Along the journey, minerals from the crust and magma dissolve into the superheated water, metals like iron and manganese that bind with sulfur to form compounds known as sulfides. When water jets from the crack it may be as hot as 400 °F or more. Only the extreme pressure weighing on the bottom of the sea prevents that water from boiling. As the scalding plume disperses, it cools rapidly: shift just a few yards from the hydrothermal vent, and temperatures approach normal. It is in this delicate transition zone, between superheated and super frigid waters, that the spiny skate stations its egg cases, where they are warmed by a natural incubator that hastens their development. Baby skates, snug in their hydrothermal cribs, hatch a little earlier than their cold-water cousins, and the tightrope act of raising your children near a roaring volcano is rewarded.

While a few other creatures use the plumes for their heat alone (some flatfishes lie in wait for an unsuspecting squid or fish to swim too close and poach themselves to death), it is the mineral soup spewed by these hydrothermal vents that supports, as if by magic, a thriving community. Until 1976 it was thought that virtually all life on Earth, or more precisely the energy of all life, must derive from the sun. Plants grow through photosynthesis, as do phytoplankton; grazing animals survive by eating those green solar factories; predators can succeed only because prey have plants or algae to eat. Even decomposers like fungi and hagfish are gnawing on the decayed remnants of sunlight. But the discovery of hydrothermal vents changed all that. Miles below the surface and thousands of feet beneath the twilight shallows, where the only food is an ephemeral drizzle of degraded organic material, astonishing hamlets of life were unveiled. Marine worms poking red heads from giant cream-colored tubes cluster by the thousands around the vent’s mouth. White crabs, hairy as yaks, crawl one upon the other like so many ants in a colony. Farther from the fissure are sea cucumbers, long-legged crabs, and round-headed miniature octopuses. To watch video from remote vehicles navigating around hydrothermal vents is to be staggered by an exuberance of life that can scarcely be comprehended.

What puzzled scientists was how that abundance could be supported, so far from the sun’s rays. The answer to the conundrum lies in the tiniest of organisms: bacteria. While photosynthesis in a plant fabricates sugars from atmospheric carbon with the power of sunlight, a few special deep-sea bacteria can power the manufacture of sugars with energy bound in chemicals pouring from the hydrothermal vent. Earth’s minerals spew forth as high-energy sulfides, typically metal atoms bound to sulfur. Huge chimneys, structures that can tower more than 100 feet tall, are formed from the clouds of minerals that pour from a vent like smoke from a chimney. Most of these smokestacks vent billows of black water, rich in sulfides of zinc, lead, and iron, giving them the nickname of black smokers.⁶⁸ After gushing from the chimney those heavy metal particles sink and settle around the vent mouth, concocting fantastical spires and twisting pinnacles, geochemical sculptures reminiscent of the visionary Spanish architect Antonin Gaudí.

Bathed by the black clouds, enterprising bacteria split metals from their sulfur partners, releasing a jolt of electricity they can harness to make sugars and starches from carbon in the surrounding seawater. These unique bacteria are known as chemoautotrophs, a tongue-twister signifying they make food (“troph”) by themselves (“auto”) solely with the energy in chemical bonds (“chemo”). But bacteria need a place to live, an apartment to settle in while they play with their chemistry sets, and they have willing landlords in deep-sea worms that evolved over millions of years into the perfect hosts.

Clustered around any hydrothermal vent, colonies of colonial tube worms bristle like white skyscrapers. The giant tube worm (Riftia pachyptila), first discovered when the bathyscaphe Alvin (modern cousin of Piccard’s Trieste) explored the newfound Galápagos hot water plumes, is one of a handful of tube worm species now known to thrive near hydrothermal vents. Distant relatives of earthworms, these 6-foot invertebrates construct a thin-walled, cylindrical case for themselves made of proteins and chitin.⁶⁹ The tube protects the resident’s delicate tissues from attack, but more importantly it allows the worm’s feeding apparatus to stretch away from the seafloor and up into the water column. Creatures like Riftia are descended from filter-feeding worms that sift tiny organic particles from the water with netlike tentacles mounted around their mouths. In hydrothermal worms, the tentacles have evolved into a carmine-colored branchial plume, an external gill folded like a taco that they use to capture a novel kind of deep-sea food: metal sulfides. Occupying most of the rest of the worm’s body is a blood-rich organ called the trophosome, a veritable apartment where chemoautotrophic bacteria comfortably reside.

In the worm’s blood, highly specialized hemoglobin molecules travel to the branchial plume, pick up a load of sulfides, and transport these invaluable packets of energy to the overcrowded apartment (which harbors nearly a trillion bacteria per gram).⁷⁰ Inside the trophosome, the chemistry begins: bacteria grab carbon dioxide, also transported by the blood, and manufacture a steady stream of small sugars, as well as key organic acids and proteins synthesized from nitrogen.⁷¹ The worm never eats a mouthful but flourishes nonetheless, thanks to a life-sustaining soup of nutrients fabricated by its symbiotic residents and absorbed without lifting a fork.

Factories of chemoautotrophic bacteria take up residence not only in worms; colonies have been found cohabitating in shrimps, mussels, and even snails.⁷² One in particular, the scaly-foot snail (Chrysomallon squamiferum, aka sea pangolin) hosts bacteria in nano-tubes jutting from scales on its foot, and as sulfurous waste puffs from each tube, it reacts with dissolved iron in the water that precipitates onto the snail’s foot as iron pyrite (otherwise known as fool’s gold).⁷³ The result is a snail fed by bacteria and encased in iron-plated armor, a double benefit. Still another beneficiary of bacterial exuberance are yeti crabs (Kiwa hirsuta) who host them on a distinctively thick, hairy coat. Comically nicknamed “Hoff crabs” for their indirect resemblance to the densely hirsute chest of bygone actor David Hasselhoff, these crabs farm luxuriant colonies of bacteria on their fur, then harvest them with a claw modified as a comb. So abundant are colonies of Hoff crabs they literally carpet the seafloor, draped over every promontory, boulder, and swale.

Surprisingly, fishes are relatively rare at such cornucopias of life, eschewing it seems the dangers of swimming near a boiling volcano of water spiked with hydrogen sulfide.⁷⁴ Still, one known as a pink eelpout (Thermarces cerberus) for its elongated shape, flat tail, and sulkily downturned mouth, wriggles between clustered vent worms, gnawing on limpets and other mollusks encrusting their tubes.⁷⁵ How the eelpout can live where earthly fires threaten to poach it at every turn—its scientific name even references the multiheaded dog guarding the Greek underworld—is anyone’s guess. Hydrothermal vents continue to yield surprises, and strange new animals are routinely discovered at these bizarre locations; after thirty years of study, two new vent species are still being described every single month.⁷⁶ Although isolated by mile after mile of cold, nutrient-poor water, those animals appear capable of colonizing distant hydrothermal vent fields. Genetic evidence suggests vent specialists may disperse by leapfrogging, probably in their larval stage, using favorable currents to reach vent sites like stepping stones across inhospitable seas.⁷⁷

All these extraordinary organisms, including tube worms, navigate a delicate and dangerous balance between the cornucopia of life afforded by superheated vent water and the freezing, hyper-pressurized sea all around them. Auguste Piccard and his bathyscaphe withstood the latter two extremes, but fishes lack the protection of a pressurized capsule. For them, the immense water pressure of the deep sea imposes harsh consequences at the cellular and subcellular level. In fish cells, fatty acids that normally keep cell membranes pliable become rubbery and inflexible under high pressure, treacherously impairing their function. Imagine if pancreatic cells could no longer pump digestive enzymes across a nearly impermeable membrane—the fish would starve. As depth increases, fish (and bacteria) dial up the proportion of polyunsaturated fats in those lipids.⁷⁸ Unsaturated fats are more flexible and fluid under pressure, thanks to kinks in their carbon backbone; for a home kitchen example, compare solid butter (rich in saturated fats) at room temperature with olive oil (mostly unsaturated) that remains liquid. Deep-sea sharks, who like their shallow water cousins rely on a fat-rich liver for buoyancy, also show increased levels of unsaturated fatty acids to keep organs and cells supple.

Housed within those liver cells, and all the body’s cells, proteins are hard at work. But the crushing pressure of the abyss also squeezes proteins during their formation, bending them dangerously out of shape and hobbling their performance. Faulty proteins are another swift highway to death, so the evolutionary pressure to solve this malfunction has been acute. Fishes of the deep sea rely on a chaperone molecule to assist protein folding and performance, as a yoga instructor might help an inflexible newcomer to stretch without injury. Called trimethylamine oxide, or TMAO for short, this mouthful of a molecule prevents extreme pressure from pinching shut a protein’s active site, the place where it binds to target molecules as precisely as a lock accepts a key.⁷⁹ While modest levels of this compound are common in shallow-water fishes (where it is responsible for the characteristic “fishy” smell), its concentration soars with depth, protecting the proteins of deepwater fishes and ensuring they keep swimming, seeing, breathing, eating, and surviving.⁸⁰ Too much of a good thing, though, can be problematic. In the case of abyssal fish, this helpful chemical may actually set a hard limit on the maximum depth at which they can survive.

Among the deepest fishes in the world are the Mariana snailfish (Pseudoliparis swirei), and an as-yet unnamed relative, both having been discovered at depths of 27,000 feet.⁸¹ A snailfish’s body is so loaded with TMAO, however, that it risks death by drowning, or at least by osmotic imbalance. Fish are normally less salty than seawater, causing them to lose water to the ocean by osmosis, the diffusion of a fluid. They replace that lost water by drinking saltwater, often while gulping prey, then eliminate excess salt across the gills. If a fish finds itself saltier than the surrounding water (as happens when oceanic salmon run up freshwater rivers), osmosis brings water into its body, which must be pumped out by its kidneys. If the pumps cannot keep up, the fish can absorb so much water that it would drown in its own juices. Osmotic calculations suggest that the amount of TMAO required to protect proteins at depths much beyond 27,000 feet is so great that no fish on Earth could survive the inrushing water.⁸² Overwhelmed kidneys would fail, and the fish would perish. The Mariana snailfish, it seems, will meet few rivals for the title of world’s deepest fish.

The Best of Both Worlds

While only a fraction of the planet’s fishes can withstand the harsh extremes of the deep, and numerous species can enjoy the shallows, there are some who have chosen an intermediate path. Vertical commuters, these fishes seek the benefit of both worlds: the relative safety afforded by hiding in the dark depths, and also the abundant food on offer in the sunlit shallows. To enjoy both realms, they make impressive daily journeys, swimming up to the surface at dusk and descending well below the twilight zone at dawn, when visual hunters emerge to terrorize shallow waters. One such daily migrant is the innocuously named cookie-cutter shark (Isistius brasiliensis). Diminutive but dangerous, these slender little sharks rarely exceed 2 feet in length. Their mouths are oddly shaped, more rounded than in their relatives, and bear slightly fleshy lips that give the appearance of having recently enjoyed a Botox treatment. Kissing, however, is not their specialty. Instead, these lips latch onto the flanks of larger fishes, whereupon a muscular pharynx applies strong suction, saw-like teeth slice into flesh, and the shark’s body swivels violently until a circular plug is removed and swallowed.⁸³ Fish, whales, and even scuba divers who have suffered such an attack bear distinctive, hockey puck-shaped divots where a painful mouthful was excised.⁸⁴ Cookie-cutters camouflage themselves against predators using bioluminescence to break up their silhouette, but they add a deceptive twist. Interrupting the broad apron of gleaming blue is a dark collar, crossing the neck. When seen from below, this stripe mimics the outline of a slender, much smaller fish or eel, luring large predators in for a closer look, and a date with the cookie monster.⁸⁵ After eating, hesitant to get caught with its proverbial hand in the proverbial jar, these sharks dive to great depths when daylight arrives. Some specimens have been recorded as deep as 12,000 feet, where they can escape the wrathful vengeance of their latest victim.⁸⁶

Lanternfishes, in whose bioluminescent glow we recently bathed, also have enjoyed tremendous success adopting the vertical commuter lifestyle. This constellation of approximately 250 species ranks among the most abundant vertebrates in the ocean: they account for some 65 percent of the deep-sea fish biomass that may tip the scales at nearly 5 gigatons (more than 11 trillion pounds).⁸⁷ Massive schools use the vertical range of ocean environments to their best advantage. By night, they ascend to the surface where they dine voraciously on copepods and other plankton, relying on huge eyes to find prey by moonlight. That rich and abundant food helps them grow quickly, and after one or two years they are ready to reproduce. As dawn breaks, they creep down into the twilight depths and flick on their belly photophores to obscure them from deepwater predators.⁸⁸ In comparison with orange roughy and other deep-sea fishery targets, lanternfishes may represent a sustainable source of fish protein, as long as their fishery is properly managed. Though the flesh is too oily to be favored by gourmands, when ground into fish meal it is delectable to salmon, tuna, and other predatory fishes reared in aquaculture ponds (about which we soon will learn more).⁸⁹ If we are to save our seas and feed a planet at the same time, deepwater lanternfishes may light the way.

Life in the deep sea is confronted by pressures, literal and figurative, that are found nowhere else on the globe, at least not today. The primordial environment around hydrothermal vents has not been seen on the planet for several billion years, when volcanoes filled a nascent atmosphere with sulfides and oceans were scalded by an unshielded sun. In 1929, John Haldane of the University of Cambridge shook the scientific world when he proposed a new theory for the origin of life on Earth: organic molecules spontaneously assembled within a “hot dilute soup” of sugars and proteins swirling in the “primitive oceans.”⁹⁰ He posited that “the first living or half living things were probably large molecules,” and then envisioned the appearance of the first primitive cell on the planet. “The cell consists of numerous half-living chemical molecules suspended in water and enclosed in an oily film.” Fifty years later, the discovery of deep-sea vents prompted NASA chemist Michael Russell to suggest abyssal sites as candidates for this hypothesized origin.⁹¹ Researchers at University College of London in 2019 added fatty acids and fatty alcohols to a simulated hydrothermal vent, and lo and behold cell membranes emerged from the stew, Haldane’s selfsame “oily film.”⁹² Fossils in oceanic crust rocks dated to 4.2 billion years ago have revealed what may be the earliest evidence of a living organism: “microscopic tubes and filaments” that resemble microbes living on today’s hydrothermal vents.⁹³ Life on planet Earth may very well have originated as chemoautotrophic bacteria that first survived on minerals gushing from hydrothermal vents, then evolved into more complex organisms which eventually colonized the seas by vaulting from one vent field to another.

Skipping from one oasis to the next, across inhospitable seas, is a common strategy in the world’s oceans. Seamount fishes leapfrog between far-flung mountaintops, whale fall specialists do the same, and dazzling coral reef fishes release eggs into currents that deliver them to distant yet comfortingly familiar reefs. It is a strategy that can lead an animal across the seas, hopscotching its way for generations from one favorable locale to the next, traveling thousands of miles from home. And not only fishes have taken advantage of this tactic to colonize new seas. Human beings in the dawn of our history followed stepping stones of their own, crossed an ocean, and ended up settling a vast new world.