^{Excerpted from WHAT A FISH KNOWS: The Inner Lives of Our Underwater Cousins by Jonathan Balcombe, published by Scientific American/Farrar, Straus and Giroux. Copyright © 2016 by Jonathan Balcombe. All rights reserved}

True to their magnificent diversity of forms, fishes exhibit a full Monty of breeding systems—thirty-two in all. They have as many different kinds of reproductive behavior and strategies as exist in all the other vertebrates combined. There are promiscuous fishes, polygamous fishes, and monogamous ones, including fishes that mate for life. Depending on a male’s sexual playbook, he may keep a harem, defend a territory, spawn in a group, engage in sneak copulations, bide his time as a satellite male, or commit acts of sexual piracy. And females are hardly passive accessories.

The great majority of fishes exhibit a familiar pattern with an obscure name, gonochorism, in which individuals are either male or female throughout life. But there are scores of fishes who cross gender lines. For some reason, reef living in particular has had a diversifying effect on sexual expression. More than one-quarter of all fishes on a reef can transition from male to female, or vice versa. Other fishes opt for a unisex approach, assuming both male and female identities simultaneously, or sequentially.

Of the species that produce both sperm and eggs at the same time (simultaneous hermaphrodites), most are found in the vast darkness of the deep sea. Being able to fertilize yourself is a very useful adaptation where the daily prospects of finding another of your kind are almost as dim as your surroundings. The sex-changing fishes (sequential hermaphrodites) are not so restricted, and they benefit by assuming different sexual identities at different ages and sizes. For example, in a mating system in which one male may monopolize many females, it pays to start out as a female, then become a male when you are large and more physically capable of rebuffing the challenges of competitors. Often, all younger members of a species are females, with a harem male occupying the top position.

In other cases, the chain of command is reversed, with a string of lesser males awaiting the future prospect of becoming a breeding female.
Clownfish (Amphiprioninae) rely on size, hierarchy, and sex change to maintain social order. They live in groups comprised of two large members and several smaller ones. The big ones are the breeding pair, the larger of whom is the breeding female. The subordinates, all males, are ranked hierarchically according to size. Although these lower-ranking fishes may be as old as the spawning pair, the behavioral dominance of the sexually mature individuals keeps the subordinates from growing or developing. When ethologist and filmmaker Hans Fricke was at the Max Planck lnstitute in Seewiesen, Germany, in the 1970s, he and his wife Simone studied this strict mating system. They described the low-ranking males as being, in essence, psychophysiologically castrated. If the breeding female dies, the chief male changes sex to female and the next largest fish in the subordinate group bumps up to chief male. So there is always hope for advancement for a suppressed male in a clownfish family.

Sex-changing fishes behave appropriately, performing male-typical or female-typical sexual behavior according to their current gender assignment. Sexual behavioral plasticity can also be observed in fishes that do not normally change sex, but who are subjected to hormonal manipulation. Results of field and laboratory observations suggest that some fishes have a sexually bipotential brain that can manage two types of behaviors, unlike most other vertebrates, which have a discrete sex differentiation of their brain and can only perform gender-typical sexual behavior.

The ability of individual fishes to change sex shows just how fluid gender divisions can be in nature. Once you know what sex you are, there is still the matter of whom to mate with. Because a sex partner supplies the other half of the genes that go into your offspring, it helps to have ways of evaluating the caliber and desirability of a prospective mate. That’s where courtship comes in. Fishes seduce prospective partners with dance sequences, love songs, and sensual touches. And, in at least one kind of fish, with artistic expression.

During a dive off the southern tip of Japan, veteran diver and photographer Yoji Ookata was surprised to see, at a depth of about eighty feet, a six-foot-wide symmetrical circular pattern in the sand. The mural featured two concentric rings of ripples radiating outward from a center disk. Ookata returned some days later with a film crew, and the mystery of what might have created this exquisite curiosity was soon solved. The geometric “crop circles” were created by a small, quite ordinary-looking male pufferfish (Tetraodontidae). Swimming on his side, while fluttering a pectoral fin, the five-inch puffer spends hours making his masterpiece. He inspects it as he goes, decorating his mural with bits of small shells that he cracks in his mouth before sprinkling them into the central grooves.

Mandalas made by other males have been found since. No two are the same. There appear to be several functions of these structures. Chiefly, they attract female puffers who, if all goes well, lay their eggs in the inner circle. The furrows help prevent eggs from being carried away by currents, and the crushed shells probably enhance this effect while providing camouflage for the eggs. Males who build more elaborate circles appear to have better mating success, which drives the evolution of this elaborate artistry.

Just as male Australian bowerbirds build complex structures to attract and impress females, so do some cichlid fishes (Cichlidae) build bowers. Lacking grasping appendages male cichlids must use their mouths to pick up and deposit sand, and their fins to shape it. Each species constructs a bower of different design, from simple depressions, to arenas with radiating spokes, to volcano-shaped sand castles projecting a foot or more from the bottom with a courting platform at the top. The height or depth of these aquatic edifices seems to advertise the male’s health and the quality of his genes. As with their distant feathered relatives, the fishes’ bowers function mainly as way stations for display, courtship, and spawning. Almost as soon as eggs are laid, females pick them up in their mouths and move to a safer brooding location.

Artistry is just one way to win a mate. Another is that familiar old tactic: deception. In the case of a female brown trout (Salmo trutta), this deceit takes the form of a fake orgasm. Having made a depression in the sand that serves as a nest, a female trout normally releases her eggs with vigorous body quivering in the presence of an amorous male. Caught up in the moment and seizing his opportunity, the nearby male follows the female’s lead, furiously quivering while releasing his sperm into the water. But sometimes he has been duped. Her own quivers were eggless. A female trout may practice this trickery to test the male’s vigor. Or, she may have decided that he is not the one for her and she seeks to draw in other males in hopes of finding a better father. This sort of reproductive conflict is common in nature. A male can afford to fertilize all of a female’s eggs with his abundant sperm, and still have more left over for other females. A female, in contrast, may do better by having several sires for her precious eggs, improving her odds that some will be fertilized by the best-quality males.

Female cardinalfishes, Apogonidae, have a scheme of their own. Males protect the female’s eggs by gingerly carrying them in their mouths. It’s a major self-sacrifice because the males must forgo eating during this critical period of the reproductive cycle. Sometimes it is just too much for a starving male to bear, and he has been known to swallow the whole egg bunch in one gulp. In a ploy to lessen the chances of this unfortunate outcome, cardinalfish mothers will lay a number of yolkless “dummy eggs” along with the real ones. Perhaps females produce so-called “trophic eggs” to reward males for their investment, with males discriminating faux eggs from fertilized ones, eating the former and saving the rest. After all, the fertilized eggs contain his investment, too.

Among the diverse cichlids of Lake Malawi, it is the males who engage in egg mimicry. Each male sports several yellow spots on his anal fin, giving the impression of a small group of eggs. A female, who deposits her eggs on a substrate before collecting them in her mouth, finds the little tail-cluster irresistible. Drawn close to the male’s reproductive organs, the female inhales most of the sperm he ejaculates, where it may better fertilize the eggs already in her mouth. Although sometimes described as an apparent visual decetion, the male’s “egg” spots probably act less as a trick than as a stimulus. Procreation is as vital to females as to males, so perhaps the female is not so much deluded as excited by the male’s seductive visual signal.

The mating behavior of a male Atlantic molly (Poecilia Mexicana) seems to vary according to the social setting; specifically, when rival males are nearby, a molly will pretend he’s attracted to someone else. Male mollies have an intromittent organ called a gonopodium—a fleshy appendage supported by a bone, which functions as a penis. A male can signal his sexual interest in a female by nipping her and thrusting his gonopodium toward her. Males being watched by rivals may act as if they prefer a formerly rejected female. They may switch from a larger to a smaller Atlantic molly or from a female of their own species to a close relative, the Amazon molly (Poecilia for-mosa). It is thought that a male molly does this with the purpose of steering his rival’s attentions away from a more desirable female. Male mollies are influenced by the preferences of rivals. By deflecting rival males’ attentions to a different female, the first male improves his odds in the sperm lottery with his preferred mate by raising the proportion of her eggs he is likely to fertilize.

There is a feminist twist to this story. Unlike their close cousins the Atlantic mollies, female Amazon mollies are an all-female species. There are a few other all-female species among reptiles, amphibians, fishes, and birds. These species are referred to as parthenogenetic because no sperm is required to fertilize their eggs. But the situation is even more peculiar in Amazon mollies, because they can produce fertile eggs only if they mate with a male molly of another species. Although the mating act is necessary to trigger pregnancy, sperm do not actually fertilize the female’s egg. The males appear to benefit by boosting their desirability to female Atlantic mollies. Several fishes, including mollies and their close relatives the guppies, are known to be trend conscious, and Atlantic females often copy the choices made by their Amazon counterparts.

Most fishes mate without penetration, but there are many exceptions. All male elasmobranchs (the sharks and rays) have claspers, paired organs that the male inserts into the female’s genital opening for sexual intercourse. Among bony fishes, males of the family that includes guppies, mollies, platys, and swordtails all possess a gonopodium. Most of the time the gonopodium is directed backward, but when needed it can be swung in different directions. Flamboyantly colored males wave their gonopodia about, apparently to impress females. Although the guppies are diminutive—most between one and two inches long—their gonopodia are about a fifth of their body length.

The priapium fishes of the appropriately named Phallostethidae (translation: chest-penis) also have penetrative sex. These fishes are small (up to 1.4 inches), humble-looking creatures, numbering twenty-three species. Par-tially translucent, they live in brackish waters of Thailand and the Philippines. They are named for a muscular, bony copulatory organ, the priapium, found under the throat of males. In some species the priapium is even accompanied by a fully functional testicle. Another feature of the priapium is a serrated hook, the ctenactinium, which grasps and holds on to the female during the sex act. Careful anatomical study confirms that this remarkably complex apparatus is derived from the missing pelvic girdle and pelvic fins. It is a testament to the importance of sex that evolution would see fit to ditch a pair of useful fins in exchange for a copulatory aid. It’s also a nod to the mystery of life that ancestors of these fishes seemed to get along perfectly well without a priapium.

Does size matter in the fish world? It seems to for mosquitofishes (Gambusia affinis), in which the gonopodium can extend to seventy percent of the length of a male’s body. The biologist Brian Langerhans, then at Washington University in St. Louis, placed a female mosquitofish into a tank and projected an image of a male on each side. One male’s gonopodium had been digitally manipulated to appear longer than the other. In every trial, the female swam toward the male with the longer organ. But ever-efficient nature poses restrictions on extravagance. Just as a peacock burdened with a tail two feet longer than the competition would be more likely to fall victim to a predator before he even had the chance to breed, mosquitofishes with larger organs are more vulnerable to their enemies. Big gonopodia produce more drag in the water, making their bearers easier to catch. Fittingly, males living in predator-infested lakes have smaller gonopodia than males in safer waters.

Numerous fish species release eggs and sperm into the water for so-called external fertilization. That style of breeding manifests in countless ways among fishes. Sea lampreys (Petromyzon marinus), for example, have complex nesting and mating behavior, which defies the “primitive” stereotype with which these ancient jawless fishes are labeled. Like salmon, they are anadromous—having both marine and freshwater stages in their life history. At spawning time, they surge upstream to build an oval nest two-to-three feet in diameter. A mated pair use their suction mouths to lift or drag stones to a pile upstream from the nest. In mating, the female grasps a rock with her mouth; the male grasps the female behind her head, then twines his body around hers;  they then both vibrate vigorously. This motion stirs up fine sand that sticks to the emerging eggs, helping them sink into the nest. Next, the parents separate and begin removing stones from above the nest and placing them on the downstream side, which performs two functions: loosening sand that further covers the eggs, and shoring up the nest cavity to secure the eggs in place. The parents repeat the whole process until all the eggs are extruded. Once preparations are completed, the pair soon die.

One of the most elegant symbioses in the oceans involves a curious sexual arrangement between bitterlings (Rhodeus amarus; small fishes of European streams) and mussels. When it comes time to mate, a female bitterling finds a suitably-sized mussel of the Unio genus in which to lay her eggs. The bitterling mother-to-be uses a long, hose-like egg-laying tube to insert her eggs into the bi-valve’s siphon, itself a tube-like structure used by the mollusk for filtering water and food. Once the eggs are inside the mussel, the male bitterling releases his sperm near the siphon entrance, some of which is inhaled by the mussel. Over the ensuing days, the bitterling’s fertilized eggs hatch and develop in the safety of their molluscan cloister. The mussel does not release the bitterling fry until its own eggs have properly ripened. The mussel’s eggs adhere temporarily to the baby fishes, which provide a convenient egg dispersal service for the mollusk.

As usual, what we know about the sexual behavior of fishes is only a fraction of the range of activity. Of those species that have been studied, many were in artificial environments, which has the advantage of convenience, but which may have the unfortunate effect of suppressing sexual behaviors readily
expressed in the wild. We may wonder what marvels await discovery, or shall remain forever hidden in the depths.

--JB