Toxic Relationships

I could not love except where Death

Was mingling his with Beauty’s breath

—Edgar Allen Poe, “Romance”

Coral reef fishes live and evolve not in isolation, but enmeshed in an intricate ballet with thousands of creatures around them. In this company, however, many of the performers are trying to eat you, and some of the tiniest stage hands can save you. Like all higher animals, pufferfishes lack the biochemical pathways to assemble tetrodotoxin. But they have drafted into service a few lower organisms that can brew the deadly potion. Puffers acquire tetrodotoxin thanks to several groups of bacteria, some hosted and some eaten. Strains of toxin-making Pseudomonas will colonize a puffer’s skin and render it poisonous,⁸ while a few types of Vibrio bacteria that also manufacture the poison are routinely absorbed from gobbled snails, shrimp, and some sea stars.⁹ During the spawning season, when predation risk soars, pufferfishes will even stock up on defensive poison by eating egg plates of flatworms (Planocera multitentaculata) that are packed with tetrodotoxin. The fishes themselves show resistance to the toxin’s effects, and they are able to re-direct the poison to their skin and internal organs, particularly the aforementioned liver. If reared on a tetrodotoxin-free aquarium diet, puffers quickly lose their toxicity, elegant proof that diet plays a key role.¹⁰ Predators learn to avoid pufferfishes since the smallest mouthful of their tetrodotoxin defense (if they even survive) teaches a nauseating and numbing lesson. Certainly Captain Cook would never again have eaten the fish that nearly killed him. So powerful is this association that even toy models only faintly resembling pufferfishes are unfailingly avoided by piscivores in research trials.¹¹

Puffers are not the only ones who have developed a degree of resistance: predators have fought back, through evolution, against this powerful defense. The best example comes from California, albeit on land, where common garter snakes hunt rough-skinned newts, the most toxic salamander in North America. Tetrodotoxin protects the newt, sequestered in skin glands; the same Pseudomonas bacteria (among others) live on its skin and are responsible for initially producing the toxin.¹² The newts evolved the ability to marshal this poison as a defense against predation, but garter snakes have had some time to develop a counter-strategy. Garters in the region show varying degrees of resistance to the toxin, and this resistance peaks in sites where newts are routinely encountered.¹³ In those same areas, the newts have fought back with higher levels of tetrodotoxin. An evolutionary arms race seems to be underway, with each species ramping up its defense and counter-defense in response to the other.

Back on the coral reef, predators and prey continue the tango of coevolution. Hunters become faster, their senses more acute. In response, the hunted have adopted a wide range of defensive strategies, from camouflage to sharp spines, armor plating to toxicity, and the interplay of offense and defense kindles the diversity of reef fishes. Like puffers, most fishes possess skin glands which secrete mucus, a protein-rich slime that reduces friction while swimming, shields against external parasites, and makes fish slippery when attacked by predators or grasped by anglers. Soapfishes, close relatives to groupers, produce so much mucus when threatened that their skin becomes covered in foam as the fish literally works itself into a lather. That soapy foam is toxic, capable of sickening or killing other fishes that come in close contact;¹⁴ it also has antibiotic properties that shield the soapfish from infection.¹⁵ Its active compound is a poison called grammistin, whose effects were discovered inadvertently by researcher John Randall. After spearing a 9-inch soapfish, he made an unwise decision: “rather than carry the fish all the way to the boat at the surface, it was stored temporarily inside [his] bathing trunks. Very soon it became apparent that a secretion from this fish was a powerful urethral irritant, and it was promptly removed from the bathing suit.”¹⁶ The defense appears successful against predators as well as foolhardy scientists, since soapfishes are rarely found in the stomachs (or trunks) of piscivores.

Many reef fishes use poison as but one deterrent in their defensive arsenal. Boxfishes, square-bodied and slow-swimming creatures with a tiny tail for propulsion, are heavily armored by a bony carapace of skeletal elements interlocking just beneath the skin. Despite an eponymously boxy outline their shape is remarkably hydrodynamic and has even been applied to experimental vehicles designed by Mercedes Benz. Yellow boxfish (Ostracion cubicum) augment their protective armor with toxic skin secretions of unique protein boxin, a hemoglobin-destroying poison three times more powerful than cyanide.¹⁷ Meanwhile, the finless sole (Pardachirus marmoratus) has been dubbed the shark-proof fish thanks to paradaxin, its own brand of toxin that serves as a powerful deterrent to sharks.¹⁸ An unhurried bottom-dweller related to flounders, the sole also relies on camouflage, hiding in plain sight on sandy or pebbled bottoms. Flounders and soles match the pattern and color of the bottom by transforming pigment skin cells into splotches of different hue and size, a disappearing act that happens in as little as 6 seconds.¹⁹ If you are small, or slow, or both, you must have formidable defenses if you are to survive. So it is not surprising that the tiniest fishes on the reef are among the most well-protected. Gobies, a group that includes the smallest vertebrate animals on Earth, rely on an impressive range of defenses—from toxins to camouflage to tunneling—and the result has been an astronomical success: the family of gobies contains more fish species than any other.²⁰

Gobies resemble miniature cylinders, tapering toward the tail, with a dorsal fin distinctively split in two parts, and pelvic fins modified into a disc-like suckers. Apart from these unifying features, roughly 2000 species present a diverse mix of habitat and diet preferences, courtship and mating ceremonies, and defenses against predation. A couple dozen species live among branching and stony corals, but most gobies have taken up residence on the bottom. In this they are aided by the lack of a swim bladder, their negative buoyancy allowing them to rest comfortably on the sand or stone. There they scuttle about capably on bent pectoral fins, looking for all the world like a fish doing push-ups. So diverse and abundant are gobies that on tropical reefs they make up a fifth of all fish species, a third of all individuals, and can account for as much as 50 percent of all the energy flow. Most measure between 2 and 4 inches in length, although the record-setting coral reef pygmy goby (Eviota sigillata) reaches only three-quarters of an inch. Being small usually correlates with a short lifespan, and here gobies are superlative as well. At least two species can expect to live no more than eight or ten weeks, the briefest blink of an eye that is another world record among marine vertebrates. They become sexually active at age five (weeks!), reproducing early to offset swift and sweeping losses to predation:²¹ annual mortality in gobies can exceed 97 percent.²² To fuel their rapid growth (granted, to a tiny finished product), gobies eat copious amounts of detritus, organic matter falling from above or cellular ejecta from sponges; many of the smallest species, however, lean toward carnivory.²³ Hyper-abundant and quick to reproduce, gobies are critical to reef food webs, assimilating nutrients and conveying them to predators (in the form of their own bodies).

Perhaps nobody informed gobies of their chief role, for they certainly try to avoid that fate. Many species have toxic skin secretions, a few even loaded with tetrodotoxin. They warn predators, with bright bands of turquoise blue or spots of maroon, that a nasty mouthful awaits. Coral-dwelling gobies (genus Gobiodon) live inside the safe refuge offered by staghorn, elkhorn, and other stony corals. As if in payment for protection, gobies fastidiously groom the coral, and will charge hungry butterflyfishes nosing about in hopes of a mouthful or two of their home. The butterflyfish soon relents, preferring to avoid castles defended by toxic palace guards.²⁴ Those guards do face one serious challenge imposed by their palatial host. Coral respiration peaks at night and uses up a lot of the available oxygen near its branches. In response, coral-dwelling gobies have a fantastic tolerance for low-oxygen conditions and will even mouth-breathe when the tide is low.²⁵ Their skin lacks scales, helping their tiny bodies absorb oxygen across the skin, but leaving them unarmored. In exchange these gobies are flush with toxic glands that slather their skin in noxious chemicals, bolstering their defenses.

Some gobies choose not to live among the parapets and ramparts of coral castles, opting instead for the sandy plains beyond the battlements. There, they thrive among reduced competition for falling food, sifting sand for tiny invertebrates, but they also face a much greater risk of predation. In response, they have learned to dig tunnels, or better yet, to hire a contractor. On tropical reefs, more than a hundred goby species have struck up a professional relationship with more than twenty species of snapping shrimp that specialize in excavation.²⁶ Known also as pistol shrimp, these crustaceans possess one oversized claw that pinches so rapidly it cavitates the water, forming bubbles and discharging an ear-splitting pop. Captive pistol shrimps held in jars have even been known to shatter the glass, so powerful is the bubble wave. The odd-couple flatmates are linked by tactile communication. While the shrimps make excellent diggers, they are completely blind. Instead, they rely on the keen eyes of the goby and use long filamentous antennae to stay in perpetual, tickling contact with the fish. Watchfully, the goby sits at the tunnel mouth, and when predators approach it flicks its tail to warn the shrimp.²⁷ It helps that some goby roommates are colored like the sandy seafloor, speckled or wrapped in pale stripes. Those simple costumes, however, are only crude examples of true camouflage, a disappearing act that our next fishes elevate to a mesmerizing art form.

Now You See Me, Now You Don’t

Flamboyant portraits of tropical fishes are painted from two entirely different palettes, each daubed with distinct types of paint. Reds, yellows, blacks, and whites are known as pigment colors and are displayed by skin cells known as chromatophores. Cells loaded with melanin, called melanophores, appear black, while those packed with uric acid are white. Xanthophores and erythrophores accumulate carotenoid pigments and are yellow, red, or intermediate shades of orange. The other palette is loaded with structural colors, reflective sheens that share more with a prism than a can of paint. Cells known as iridophores contain plate-like crystals of guanine—the much-valued fertilizer ingredient—that reflect light off the top and bottom of the plate simultaneously. Interference between the two reflections creates shimmery colors of silver, green, and blue. Most fishes have several of these cell types, often working in concert. A reflective iridophore of blue overlaying a pigment cell of yellow, for example, will combine to produce a shiny metallic green. Sometimes during a fish’s embryonic development these cells even interact. White and black pigment cells in some fishes mutually repel one another, producing alternating stripes like a zebra. More remarkable was the discovery that both pigment and structural cells can modify the intensity and even color they broadcast, sometimes in a matter of seconds. The result is a magical ability made famous in literature from H. G. Wells to Harry Potter: the power to become invisible.

Inside iridophore cells the guanine crystal layers can be distorted, altering their orientation and thickness, and shifting both color and reflective brilliance. A shimmering blue damselfish (Chrysiptera cyanea) can become dull green in a matter of seconds.²⁸ This “now you see me, now you don’t” strategy allows a fish to appear attractive to choosy partners, but swiftly throw a cloak over its vivid attire if a predator passes through the neighborhood. Pipefishes, endearing and elongate relatives of seahorses, share the same technique: a female broadnose pipefish (Syngnathus typhle) displays bright ornamentation during courtship but flips the switch to dim her embellishments when hungry cod enter the mating arena.²⁹ More impressive still are the changes that chromatophores can express. When pigments within each cell are clustered into thick dots the skin appears dark, but when they are dispersed into tiny pinpricks, the skin looks white or even translucent.³⁰ If chromatophores of different color classes alter their pigments in harmony, a fish can transform from red to yellow or from white to blue, in a matter of seconds. Localized modifications will trigger brilliant stripes to appear, flaming spots to vanish, or appealing bars of black and white to fade. Wielded together, chromatophores and iridophores can conjure a mesmerizing array of patterns and colors, and some fishes have such finely tuned control that they flawlessly mimic the backdrop and literally vanish before your very eyes.

Among reef fishes, the champions of camouflage must be flounders. These oddly shaped animals are actually compressed, their bodies flattened side-to-side, but they swim with one side always toward the bottom, making them appear squeezed from top-to-bottom (a form known technically, but forlornly, as depressed). They acquire this tilted-over orientation during larval development, a metamorphosis that involves some shocking alterations. The eye destined to look at the bottom slowly migrates all the way across the head, until it comes to rest next to the other; thus both eyes lie improbably on the fish’s uppermost side. Clearly, one can see approaching predators better this way than with one peeper buried in the mud. Flounders are separated into left-eye and right-eye species depending on which one remained fixed in place. Pectoral and pelvic fins on the lower side are much reduced, and even absent in some species. Flounders feed on invertebrates and small fishes, spending most of their time scouring sandy and silty seafloors for buried crustaceans and worms. In these open plains, they are at great risk of predation, a danger that has honed their ability to disappear. When a threat appears, they glide to an immediate halt and adopt the precise color and pattern of the bottom beneath them. They can mimic finely speckled yellow sand, smooth reddish mud, and even the coarse grey and green splotches of seafloor pebbles. One tropical species, the eyed flounder (Bothus ocellatus) can marshal the entire transformation in just 2–8 seconds, thanks to its nimble chromatophores.³¹ To simplify their disappearing act, flounders favor substrates they can readily mimic and avoid hard-to-match patterns like live coral and sponges.³² The advanced skill of copying living backgrounds is what puts our next magicians in a class all their own.

Frogfishes are possibly the weirdest looking, most improbable creatures on a coral reef. They barely resemble a fish at all. Instead of the sleek disc of a butterflyfish or streamlined torpedo of a tuna, they are lumpy and irregular, clumsy and slow, yet utterly and whimsically lovable. Fins are mounted on thick lobes, the blunt face and rounded body appear lopsided, and a downturned mouth lends them a charmingly grumpy appearance. Distinct from the similarly named but more musical toadfishes, frogfishes thrive in places that flounders avoid: they specialize in mimicry of live corals and sponges. So perfect is their camouflage that they are rarely seen, despite being quite common. One could spend an hour examining a few blobs of red sponge and never realize that one blob was actually a fish nestled against the sponge and cloaked in perfectly matching tones. Frogfishes do not adjust their coloration as rapidly as flounders, preferring instead to settle on a color pattern and stick to the background it matches. If forced to migrate, it takes a few hours to change their costume. They can match corals and sponges of vivid yellow and red, or display multicolored mottling typical of coral walls dotted with algae and invertebrates.³³ Some species are even adorned with fleshy tubercles and flaps to further break up their outline, none more so than the sargassumfish (Histrio histrio). This little magician specializes in mimicking the speckled fronds of sargassum weed, a tropical seaweed that floats on the surface in tousled masses. Concealed in this tangle of yellow and brown algae, the sargassumfish is undetectable even to its prey, tiny shrimp and larval fishes whom it lures by jiggling a worm-like extension of its dorsal fin. So theatrical is the performance that the fish’s scientific name references (twice!) an overly dramatic stage actor. Or perhaps it was the discovery of their histrionic habit of gobbling juveniles of their own species, nothing being more melodramatic than a cannibal in camouflage.

Intermediate between frogfishes and flounders, and earning honorable mention in the category of weirdest fish, are batfishes. Unlike bats they do not fly, but unlike fishes they rarely swim; instead, batfishes prefer to walk. Around eighty species inhabit tropical reefs, where they rest their flattened, triangular bodies on the bottom, perched on stout pectorals that resemble arms more than fins. Patiently they wait, tempting prey to approach by dangling a retractable lure in front of their jaws. The two-part lure, formed of a dorsal fin spine tipped with a fleshy knob called an esca, is similar to those dangled by deep sea anglerfishes, close relatives to both bat and frog fishes. Unlike their abyssal cousins, however, the batfish’s lure is not illuminated, although the polka-dot batfish (Ogcocephalus cubifrons) does employ a chemical bait to attract its lunch.³⁴ Secretory cells in the esca, not unlike those in the skin of soapfishes, exude a compound that attracts marine snails. Large numbers of their shells can be found in batfish stomachs, where they make up nearly half the contents, a testament to the bait’s appeal.³⁵ Batfishes even take advantage of underwater currents, facing down-current so the chemical temptation streams away from them like a fishing line, reeling snails to a toothy end.³⁶

Camouflage is a defense found most commonly among slow-swimming fishes who risk murder whenever they move, even within their tiny territories. None are more effective at this strategy of hiding in place than the most famous parental care iconoclasts in the ocean, seahorses. Some 25 million years ago, tectonic uplift created vast basins of shallow, warm water where seagrasses proliferated. And in those marine meadows, seahorses evolved their curiously equine shape.³⁷ Their ancestors the pipefishes swim in a standard fashion, head first like a tiny barracuda. But in the dense blades of seagrass, a new opportunity for camouflage arose. Taking full advantage, seahorses evolved an upright posture, the better to mimic the vertical blades, and a grasping tail, the better to anchor themselves to the stalks. Pipefishes were already good camouflage artists, and their ability to match background colors and patterns was supercharged in seahorses. Today, nearly fifty species thrive in the world’s oceans, pastured amid seagrasses, seaweeds, corals, or sponges against which their odd shape and superb color matching render them undetectable.

Seahorses settled into their new habitat and posture, but continued to adapt rapidly thanks to higher rates of protein and gene evolution than occur in most fishes.³⁸ They have evolved unique armor, a novel tail design, and a one-of-a-kind technique for catching their prey. Instead of scales, seahorses are wrapped with overlapping bony plates beneath their skin; so stiff is this armor that the fishes evolutionarily jettisoned their ribs as unnecessary structural supports. The tail, lacking a terminal fin, is one of the few square tails in the animal kingdom. Inside are a stack of bony squares like picture frames, each linked to the other by three distinct kinds of joints: ball-and-socket, peg-and-socket, and gliding. These joints permit a remarkable degree of flexibility, and the tail can grasp seagrasses and seaweeds as effectively as a monkey’s tail clutches a branch, curling through more than two full revolutions. Three-dimensional models of the picture frame arrangement show square seahorse tails also offer greater resistance to crushing than a comparable round tail, very useful against the jaws of fishes and bills of wading birds.³⁹ Engineers responsible for that study recommended adapting the design to medical or robotics applications, and researchers in Japan galloped with the suggestion, manufacturing a meter-long wearable tail whose wagging movements can help people counteract balance disorders.⁴⁰

While clasping seagrasses or corals, seahorses are on the lookout for planktonic invertebrates, like tiny shrimp and jumpy copepods. When it spies a suitable morsel, the seahorse moves its long snout ever so slowly into position. Research by fluid dynamics engineers revealed the seahorse’s head shape minimizes disturbance of the water around it, allowing the fish to gingerly advance its snout toward the copepod without setting off any alarms, to as close as four one-hundredths of an inch.⁴¹ Then the seahorse lunges, using a pivot-and-suction motion unique among fishes. Were it not for the stealthy approach, the copepod would escape, but because the ambush is launched from exceptionally close range, the seahorse is able to slurp prey at will, all from the security of its seagrass perch. So effective is this feeding skill that seahorses lost their teeth several million years ago, and like a high schooler after a wisdom tooth removal, they simply eat their meals through a straw.

After kangaroos, seahorses probably have the most famous pouches in the animal kingdom. Unlike Australia’s hopping marsupials, however, it is the doting fathers who bear the young. Seahorses reside in compact territories, often as little as one foot in diameter. They are highly monogamous, thought to be an adaptation to increasing reproductive success for low mobility fishes who live far from one another: better to pair with a single partner than risk wooing new mates again and again.⁴² During courtship a female (call her Helen) will travel to visit her mate every day at dawn (call him Paris, for those who remember Greek history).⁴³ On one magical morning, both seahorses begin to brighten in color and engage in reciprocal quivering, trembling and twisting their bodies, a dance that indicates their readiness. The next day is the big one. While Helen points her body toward Paris, he repeatedly opens his pouch and pumps water in and out. This action helps oxygenate the space where eggs will soon be placed. In some species, the male also makes a clicking sound while pumping, serenading his partner.⁴⁴ After a few rounds of pointing, brightening, and proud pouch pumping, Paris and Helen let go of their shared perch and rise in the water column. While drifting upward, Helen transfers her eggs into Paris’ pouch; these copulation rises are repeated several times, until anywhere from a hundred to a thousand eggs are delivered.

After receiving Helen’s eggs, Paris fertilizes them, his sperm slipping through the pouch opening before it is drawn shut. Inside, the eggs benefit from oxygen and nutrition supplied by his pouch. Genetic studies have revealed pregnancies are astonishingly similar between seahorses and humans, with dozens of shared genes that regulate nutrient transport, gas exchange, salt balance, and immunological protection.⁴⁵ Throughout gestation, which lasts from ten to forty days (depending on the species), Helen faithfully visits Paris every morning until the eggs hatch and seahorse colts trot into the open water.⁴⁶ His camouflage protects him while the couple await the glorious day, and holding eggs internally safeguards them from predators until they hatch.

Sadly, adult seahorses face heavy predation themselves, from a voracious species known as Homo sapiens. Seahorses are swept up as accidental bycatch, particularly by bottom trawlers, an indiscriminate practice from which camouflage cannot save them. One study estimated seahorse bycatch at 37 million animals per year, in just twenty-two countries with large fishing fleets.⁴⁷ But millions more are actively collected and sold in a dodgy Chinese medicine trade, where they are reputed (with no substantiating evidence) to cure everything from asthma to incontinence to impotence. Asian markets are not the only culprits, however, as some 65,000 dried seahorses are sold annually in the United States as “curios” for seaside tourists;⁴⁸ similar numbers have been recorded in Portugal and elsewhere.⁴⁹ One hopes that people will put a halt to these callous practices; exquisite and gentle seahorses deserve better.

It Takes Two to Tango

And hand in hand, on the edge of the sand,

They danced by the light of the moon

—Edward Lear, “The Owl and the Pussycat”

In Homer’s epics the Iliad and Odyssey, a star-crossed affair between Paris and Helen (the people, not the seahorses) changed the course of history when incensed Greeks laid siege to Troy for ten years, snuck through the battlements in a horse of wood, and sacked the city, leaving behind nothing but ashes. In politics, the power of love can be awesome, indeed; on coral reefs, the urge to pair and reproduce is no less a potent force in evolution. As much as avoiding predation has driven the diversification of reef fishes, courtship and mating have played an equally central role.

Most reef fishes spawn in locations with prevailing currents that carry eggs away from the reef, into deep waters where predators and planktivores are less abundant and the chance for survival is higher. No morsel is more defenseless than a tiny fish egg or newly hatched larva bobbing in the sea. Only a miniscule fraction of planktonic larvae will survive this hazardous phase of their lives. In silvery-sided jack mackerels, for example, fewer than one offspring in 50,000 live beyond their second month.⁵⁰ Such prodigious losses have propelled fishes to find new strategies to reduce risks, and new forms of communication to coordinate care. As we have seen, toadfish and triggerfish males construct nests where eggs are guarded by one or both parents. Many damselfishes engage in this modest level of parental investment, often accompanied by striking color changes to improve the guard’s camouflage. A few damsel species (in the genus Altrichthys) even defend their offspring after they hatch, patrolling tirelessly against predators. These attentive parents lack some child-recognition skills, however, as they will unwittingly serve as bodyguards for offspring of different parents, or even of different species. Genetic analyses in Philippine reefs showed two other (nonpatrolling) species have learned to drop their own toddlers into the defender daycare, just as cuckoos will lay eggs in another bird’s nest to parasitize the parenting benefits.⁵¹

Once you have built a tiny nest on a sprawling coral reef, how do you manage to draw egg-laying females to it? Visual communication, practiced by parrotfishes and a great many brightly colored reef species, attracts females and allows them to judge the vigor of their male suitors. Some species invert the courtship, with males choosing females on the basis of size, as larger fishes lay more eggs than smaller contenders.⁵² Vivid females can also be extra appealing to males, as intense colors signify a good diet and overall health. Two-spotted goby (Pomatoschistus flavescens) females with dazzling orange bellies, for example, attract four times the amount of male attention as goby gals who lack a glowing gut.⁵³ A number of fishes, particularly cryptic species, also rely on chemical attraction to seduce their partners. Those perfumes send important signals about the sexual receptiveness and location of a willing male (perhaps with a newly constructed nest site), or they serve as a calling card identifying the sender’s gender. In Gulf pipefish (Syngnathus scovelli), who also have inverted courtship, females alone release a scent that alerts nearby males to their readiness for egg-laying.⁵⁴ Blind gobies (Typhlogobius californiensis), who cohabitate with sighted shrimps in a twist on the usual shrimp-goby tale, live in little caves off the California coast, waiting for a mate. When a visitor approaches the burrow’s entrance, they sniff their caller’s fragrance to distinguish between a same-sex rival and an opposite-sex suitor.⁵⁵

Like gobies, blennies are small bottom-dwellers who scramble across sand and rocks, walking on their pectoral fins while searching for mouthfuls of small invertebrates or stray detritus. They are distinguished from their goby cousins by a dorsal fin with one or three, not two, lobes. Some 900 species can be found in oceans, and even some freshwater locales, where they adopt an impressive range of body sizes and colorations. Most species rely on camouflage for some protection, and many take up residence in small caves or holes for protection. Barnacle blennies (several species in the genus Acanthemblemaria) charmingly convert empty barnacle shells into their very own tiny houses, from which they peer out at the world with comically bulging eyes. That their eyes are further decorated with eyelash-like tentacles only adds to their cartoonish, come-hither appeal. Many blennies live out their days in extremely restricted territories, like seahorses, which can make it difficult to simply bump into a passing female, much less one who is reproductively receptive. But perfumes can help increase their chances.

In combtooth blennies (some 300 reef-dwelling species), males attract potential mates with colorful costumery, but they possess an added embellishment: twin scent glands near their anal fins. Male peacock blennies (Salaria pavo) engage in intricate courtship dances, with much raising and lowering of a rubbery, tangerine head crest that contrasts with their electric-blue striped body. Males defend territories around a nest installed in a small hole or crevice. To put females in the front row for the big performance, the males release powerful pheromones from their scent glands. Males with higher testosterone levels develop larger glands and are more committed to nest-guarding, suggesting the scent they release may communicate more to mates than simply the showtime.⁵⁶ Once eggs are laid in the nest, peacock and closely related redlip blennies (Ophioblennius atlanticus) have been observed smearing their eggs with a mucus from anal glands, a gel with antimicrobial powers.⁵⁷ Given that unguarded eggs can be destroyed by infection as readily as by a predator, this defensive behavior is another ingenious effort by parents to enhance their reproductive success.

It should come as no surprise that fishes can communicate by perfume. Marinating in water, they constantly shed mucus, urine and salts, amino acids and peptides, and so many other chemicals that one marine biologist described fishes as “leaky bags of body odor,” an expression that really puts the ick in ichthyology.⁵⁸ Fishes at the peak of breeding season are extremely responsive to this mix of communication signals. Hormones circulating within males and females ramp up as the mating season approaches and amp up auditory, visual, and chemical enticements. Atlantic salmon (Salmo salar), among other species, even release some of those hormones into the water where they serve as enticing pheromone signals.⁵⁹ Female damselfishes and midshipmen (close cousins to toadfish) become more sensitive to male courtship songs when they are reproductively receptive, and both cycles are modulated by hormones.⁶⁰ According to Karen Maruska, from whom we heard in the preceding chapter about damselfish song, chemical signals have similar effects in fishes and human beings. “Steroid hormones, estradiol in particular, improve auditory function. That’s actually true of people, too. If you look at women across the menstrual cycle … because of the levels of circulating hormones they have different auditory perception.”⁶¹ In effect, females have hormone-mediated hearing aids that crank up the volume when they are eager to hear serenading males. Male fishes (and boyfriends) may rejoice to know that when their partner turns a deaf ear on a lengthy monologue, it might be due to hormones rather than sheer boredom.

After courtship and egg-laying and fertilization, the lottery of life begins. Some eggs will be eaten, though fewer if they are guarded. Larvae hatch and are swept away from the reef to fend for themselves in open water, bobbing about near the surface where phytoplankton provide a verdant pasture during the early days of development. But eventually those larvae metamorphose into juveniles who must find their way back to a reef where they can settle into adulthood and start the reproductive cycle over. To do this, juvenile reef fishes listen and smell for clues that indicate a reef’s location, and even its makeup. While still in the larval stage, reef fishes can orient to the sounds of a coral reef nearly a mile away⁶² and swim vigorously to the source.⁶³ Cardinalfishes (small nocturnal reef dwellers named for their red colors) home in on scent plumes that drain from warm coral lagoons, sniffing the water with olfactory systems already keenly sensitive at an early age.⁶⁴ Damselfish juveniles may be even more selective, as they actively prefer waters laced with the scent of adult damsels, but crucially not the odor of close relatives, a cocktail of chemical cues pointing the way to healthy reefs that lack direct competitors.⁶⁵ Reef fishes can even detect smells that originate outside the ocean. In a study of clownfish settlement, researchers showed that larvae of at least one species (Amphiprion percula) of these adorable anemone-dwellers can detect not only a coral reef, but also a reef adjacent to a tropical island. They do this by discriminating the specific fragrance of leaves that have fallen into the water and use the scent cue when house hunting to choose only an anemone home that boasts an island view.⁶⁶ Location, as they say, is everything.

The Art of Negotiation

Only now are scientists thinking seriously about how parasites may be as important to ecosystems as lions and leopards … and perhaps the dominant force in the evolution of life.

—Carl Zimmer, Parasite Rex

More weird behaviors and wonderful fishes are found in coral reefs than anywhere else in the ocean, save perhaps in the abyssal depths. Reefs are like rainforests, where so many species co-mingle and interact that the foremost pressures of evolution come from other living organisms, rather than the nonliving environment. Species are continuously coadapting, in feedback loops that spawn towering biodiversity and provoke fascinating behaviors. Reactions between prey and their predators, and courtship between males and females, are just two such evolutionary feedback loops. But around coral reefs, interactions can occur between almost any pair of species, and even the unlikeliest of companions can make for fine bedfellows.

Take sea anemones, for instance. They are a cantankerous lot, waving tentacles packed with stinging cells that fire poison-tipped harpoons into prey and interlopers with equal ferocity. But nestled amongst those tentacles, as cozy as a kitten on a couch, one can find a clownfish or two living quite contentedly. Thrust into stardom by the feature film Finding Nemo, about thirty species of these bright orange fishes with radiant blue bars enjoy a convivial mutualism with anemones throughout the tropics. Also known as anemonefish, they benefit from the protection of their host’s stinging tentacles and feast on some of the food ensnared by the landlord. In return, the fish’s nitrogen-rich feces help fertilize the anemone. A clownfish’s rental agreement includes pugilistically defending the anemone from tentacle-eaters like butterflyfishes. They also chase off three-spot humbugs (Dascyllus trimaculatus), small damselfish relatives who love nothing better than to couch-surf in their anemone pad without paying rent. Clownfishes win that tussle most of the time but eventually fall victim to their own success. As they fertilize their host anemone, it grows larger, eventually reaching a size where evicting a gate-crashing humbug is not worth the trouble.⁶⁷ Both fishes eventually reach a disgruntled détente, like grumpy neighbors in a large apartment building. Bah humbug, indeed.

Clownfishes begin their anemone residence early in life, shortly after settling on the reef from open water. As juveniles, their bodies are covered in a thick mucus, three to four times thicker than other fishes, which gives them an initial degree of protection against the stinging cells.⁶⁸ But they shortly begin rubbing themselves against the tentacles and pick up some of the secretions of the anemone itself. Soon, they smell like their anemone host, whose tentacles no longer find them to be foreign: no amount of contact will now fire the stinging cells. By the time they reach adulthood, the microbiome of their skin mucus is significantly different from that of clownfishes not hosted by anemones.⁶⁹ That difference fades if the clownfish (in this study, Amphiprion clarkii) is experimentally evicted, evidence that regular contact with tentacle mucus is necessary to recharge the fish’s immunity. This mutualism with sea anemones drove a rapid diversification of clownfish, starting around 5 million years ago, once a few ancestral fishes adapted to life with their hosts: smaller bodies, shorter fins, and more skin mucus. Now, a unique cluster of species can be found in any coral-rich region, each one specializing in a select group of anemones, but genetically distinct from bands living on reefs a few hundred miles away.

Sometimes the benefits of a mutualism between animals can be hard to see, unless you know just how to look. Take a couple of other humbugs, known as whitetail and marginate dascyllus (Dascyllus aruanus and D. marginatus). These attractively marked fishes reach just 2 or 3 inches in length, and they associate with stony, compact corals sometimes called cat’s paws. Resembling a cluster of stubby, branching fingers, these corals live in shallow and brightly lit waters where their symbiotic algae churn out sugars and oxygen. Quite a few humbugs will live between the fingers, depending on the size of the coral colony, and provide many of the same benefits as clownfishes to anemones: fertilization with feces, and defense against corallivores like the dreaded crown-of-thorns starfish. Once darkness descends, the humbugs settle down amid the fingers, but their sleep is fitful. Unlike most crevice-dwelling fishes, these humbugs vigorously flap their fins all night long: they are sleep-swimming.⁷⁰ Careful measurements reveal that the finning aerates the coral, just as their tissues are consuming oxygen in the water layer adjacent to the stony fingers. Without humbugs corals can use up 90 percent of the oxygen in that water, which is not replenished until morning light switches on the algae. But with a troupe of finning fishes providing ventilation, the water retains as much as 80 percent of its daytime oxygen. Soft corals, which are not frozen in place by a cement exoskeleton, pulse their tentacles for this very reason, something first noticed (but not understood) by French naturalist Lamarck some 200 years ago.⁷¹ Hard corals with ventilator humbugs grow more quickly, host more algae with elevated photosynthesis rates,⁷² and even produce more eggs than colonies without fishes-in-residence.⁷³ Although the gases wafted by sleep-finning fish are invisible, the benefits to the coral certainly are not.

Swirling above the canopy of the Amazon rainforest, a rainbow of birds collaborate to find fruits, watch for predators, and navigate through broccoli-shaped tree crowns. Mixed-species flocks are common there, so long as the benefits of partnership outweigh the detriments of competition. The same phenomenon plays out on the plains of the Serengeti, where a dozen species of mammals forage together, each browsing on slightly different plants, and all keeping eyes peeled for prowling lions. In coral reefs, too, mixed-species mutualisms abound when the advantages exceed the risks. A notable case is the diverse party that accompanies a day octopus (Octopus cyanea) on its rounds, one of the most complex examples of collaborative hunting and division of labor seen in the ocean. The hungry octopus scrambles over the reef, probing coral and rock crevices with slinky tentacles in search of hidden prey, from small fishes to sea snails, clams to crabs, marine worms to shrimp. Meanwhile, swimming in orbit, a compact solar system of partner fishes scour the surroundings, each engaging its own unique skill set.

Goatfish species like the yellow-saddle (Parupeneus cyclostomus) comb the bottom nearby, using sensitive barbels dangling from their chin to sniff for buried mollusks and crustaceans. Smooth cornetfish (Fistularia commersonii) hover a few inches above, sharp-eyed lookouts for any prey fleeing through the water column. Tailspot squirrelfish (Sargocentron caudimaculatum) hang about opportunistically, and a blacktip grouper (Epinephelus fasciatus) will join and use fin and body gestures to point out hidden targets. More than a dozen species have been seen in hunting packs with the octopus, and when foraging together the fishes were able to strike prey more frequently, and more successfully, than when hunting alone. But the pack’s interactions are not always congenial. To show who is boss, the day octopus has been known to throw a punch. It balls up the tip of a tentacle into a fist, and with an explosive motion it can sock a fish right in the chops, or flank. The octopus uses punching as a partner control mechanism, warding off the squirrelfishes who contribute too little to the hunting party, for example, or warning a usually collaborative member against stealing prey.⁷⁴ The punching bag never retaliates, and fisticuffs do not break out among other members of the pack, who park their aggression when joining the hunting collaborative. This curiously selfless act of suspending hostility also characterizes one of the most spellbinding sites on any coral reef, where mixed-species flocks rival the rainforest in color and complexity: a fish cleaning station.

Fish are under constant assault, day and night, not just from hulking predators but also from tiny, vicious parasites. Worms, protozoans, leeches, and crustaceans may invade a fish’s innards or gills, or colonize its skin and scales, to steal energy and nutrition like a tick on a dog. Fish go to great lengths to ward off these pests, including slathering themselves with bug repellent made from toxins secreted by their skin.⁷⁵ But on a reef there is no better way to get rid of parasites than to visit a cleaning station. There, like enthusiastic spa staff, a crowd of small fishes and an occasional shrimp or crab scour their larger clients, plucking parasites from the scales, fins, and even the interior of their mouths. Itchy customers go to great lengths to solicit the spa treatment. Lexa Grutter from the University of Queensland has spent years studying the interaction between clients and cleaners on Australia’s Great Barrier Reef. She notes that customers often pose in “unusual postures where they open their mouths, they spread their fins out, they stay in the same spot and try to balance, and sometimes they end up upside down … and actually can look quite funny at times.”⁷⁶ She speaks poetically of the relationship between the two fishes. “It is such an intimate interaction, when you think about it. Here’s this fish that is just allowing this other animal to literally crawl over it, even climb into its mouth. I’ve seen it go into the mouth of a big giant potato cod, I’ve even seen it pop out through the gill opening. They’ll clean their eyeballs and pick at their nostrils, it’s just very intimate.”

Among the most energetic cleaners are wrasses, cylindrical and highly decorated little fishes closely related to heftier parrotfish. Dr. Grutter has shown that their bright colors, often electric blues and yellows, signal their cleaner status to incoming fish and defuse the groomer’s risk of being swallowed.⁷⁷ The small size of wrasses permits easy access to clients’ mouths, where they scrutinize teeth, tongue, and palate with the zeal of a dental student. Cleaners also attend sharks, giant rays, and even sea turtles who accumulate an irritating crust of parasites during weeks on the high sea. After a few minutes of brisk attention, the customer is deparasitized and healthy, and the wrasses have full bellies. Spa treatment completed, the client is given a hot towel and shown the door, and the next fish in line glides into the salon. On reefs with readily available cleaning stations, groomed fishes are healthier, have lower stress levels, and grow larger, all benefits that outweigh the miniscule value of swallowing your masseuse.

Grutter’s unique career was inspired in part by a childhood spent in Alaska with her mother and father, a deep-water fisherman. She vividly recalls gutting some of the day’s catch and curiously examining their internal organs, only to find a few salmon and halibut repulsively loaded with parasites. Unnervingly, she notes how widespread parasites can be. “It’s one of the most common life forms on the planet. We all have parasites, we’re crawling with parasites, and we do all kinds of things to prevent it. As humans, we take showers and cut our hair and wash our clothes. Animals, they engage in grooming behaviors, they groom each other, cats clean themselves constantly. Fish, on the other hand, they can’t really groom themselves, and so they have found other ways to deal with their external parasites … they’ve somehow worked out that these cleaner organisms are interested in these parasites as food.” Cleaners can obtain quite a steady diet from their flea-ridden clients. During her tireless observations of the bluestreak cleaner wrasse (Labroides dimidiatus) Grutter showed that a single fish can pluck more than 1200 parasites in a day, an impressive feat for a fish only 4 inches long.⁷⁸ During that same day they may see as many as 2000 customers come through the spa door, with some individuals returning more than a hundred times.

Chief among the plucked parasites are gnathiid isopods (pronounced “nay-thid”), tiny crustaceans that behave like marine mosquitoes, stabbing a hole into a fish’s skin and sucking blood. Unchecked, these vampires can drain an astonishing 85 percent of a fish’s blood.⁷⁹ If the victims don’t avail themselves of a cleaning service, they can perish from the isopods themselves, or indirectly from blood diseases they often transmit. Parasitized damselfishes swim more slowly and use more oxygen, for example, and juveniles with even a single gnathiid are more likely to disappear from the reef than establish a homestead. Grutter’s long hours underwater have revealed just how important a cleaning station can be. “A rabbitfish, he went there every five minutes on average, for an entire day. The rabbitfish would be feeding on algae, and it would take a few minutes of bites and then off it went back to the cleaning station, got cleaned, came back and kept feeding.”

While clients desperately need cleaning, and cleaners must eat, this intimate interaction is not without its dangers and deceptions. Cleaners, whether they are fishes or delicate shrimps, put themselves at risk when approaching a large fish. Their very lives depend on the restraint of the potato cod, who might fancy a wrasse as an appetizer. On the other hand, it turns out that parasites are not actually the cleaners’ favorite food; they prefer to munch on the protein-rich mucus that envelops most fishes, and even the skin itself. If they begin nibbling at the mucus, though, or bite off a piece of skin, the client may get grumpy and depart in a huff, or even try to swallow the cleaner. Since either party can shatter the cleaning station’s peace treaty, they have developed ways to reassure their willingness to play nice. Clients adopt funny, head-down poses to signal their readiness to be groomed. Cleaners often preface a session with a tickling dance, brushing the client repeatedly with their fins, to soothe the customer and discourage them from taking a murderous gulp. Grutter describes the value of this tactile interaction: “It’s used to communicate with the client, and to manipulate the behavior of the client. They will use it to get clients to stay longer, and it also seems to be used to appease the client. For example, if it’s a predator, they seem to do it more so, and they did it more when they had a hungry predator than when it was a well-fed one.” A sort of safety zone develops around cleaning stations, where clients and cleaners treat each other with respect, and where even the clients desist from eating one another while waiting their turn at the spa.⁸⁰

Still, cheaters can invade the station, slinking in for their own nefarious purposes. Wrasses dress in cobalt and sunflower to advertise their services, but those colors are readily mimicked. Among any cloud of Grutter’s cleaner wrasses you can usually find a tiny bluestriped fangblenny or (Plagiotremus rhinorhynchos) or sabertooth blenny (P. azaleus), only just distinguished by their distinctive, eel-like swimming style. These little pests sometimes slip into a cleaning station unnoticed, and take a painful bite of scales, skin, and mucus. Before the chomped client can whirl in anger, they scurry away to safety. An uneasy balance exists, however, since too many biting blennies would permanently undermine the faith of customers in the safety of their neighborhood spa. As it is, infrequent visitors to cleaning stations where sabretooth blennies lurk typically will abandon the site, the very definition of the old saying “once bitten, twice shy.”⁸¹ Regular customers, though, will chase the offending blenny aggressively and return for more cleaning. Wrasses have learned these patterns and will leap to attend an infrequent visitor while shoving a regular customer off to the proverbial waiting room, confident that they are less likely to leave the spa in a sulk. In experiments where participants must adopt this so-called delayed reward strategy—servicing the antsy visitor before the faithful regular—cleaner wrasses master the optimal tactic faster than chimpanzees, capuchin monkeys, and even orangutans.⁸²

Not everything is rosy on the coral reefs. Global climate change is warming oceans, and warm waters cause corals to suffer mass bleaching events. Corals expel their symbiotic algae when thermally stressed, losing the power of photosynthesis and turning white in the process. Grutter noticed that cleaner fish were also disappearing from those bleached reefs. “We’re looking at the parasites, the client fish, the cleaners themselves, and the habitat. We can see the changes over time. Hot water temperatures don’t just affect the corals, they affect the rest of the reef community in a cascade.” Alarm bells first sounded in 1998, when unprecedented warming led to the demise of nearly one-tenth of the world’s corals. Some recovery followed, but subsequent warming events killed around 14 percent of corals in the ocean and prompted a 20 percent increase in algae cover.⁸³ The one bright spot is in the famed Coral Triangle, ancient seas between Australia, Malaysia, and the Philippines, where more than 500 types of coral and thousands of fish species make their homes. In those highly diverse waters, coral cover actually increased slightly since 1983. Supporting nearly a third of all reefs on the planet, the shallow seas of the Coral Triangle may be protected by a long history of exposure to warm temperatures, and by the adaptability of their biodiversity. Here, for the time being at least, the myriad interactions between species may be saving the reef.

The reach of global warming is long, and it affects not only shallow water reefs, but even the cold waters of temperate and polar seas. There in those productive latitudes swim some of the world’s most important food fishes. Immense schools of cod, haddock, pollock, and halibut feed millions upon millions of people around the world. They have been served with chips to British diners for centuries, been dried and salted by Norwegians, and made millionaires of many a New Englander. Their prodigious bounty has sustained civilizations, lured ancient mariners to cross oceans, and provoked wars on the high seas. And yet we are only just now discovering how these fishes live and learning to manage the fisheries that deliver their abundance to our plates.