When you’re watching a thundering plain of ten thousand migrating caribou or an oil spill–sized mega-school of five million anchovies, it’s easy to forget that each and every mammal and fish within those groups is an individual, singular in age, sex, and size. The diversity within herds, flocks, and shoals includes differences in levels of attraction and desire. Not every female caribou is interested in mating with every male. Male starlings are not attracted to every female in the murmuration. Even fish have what veterinarians would call “partner preference.”
We humans call it chemistry.
A short truck ride away from the Ohio lake at the Wilds where Milu deer practice adorning their antlers lives a population of cheetahs. The Wilds is one of nine centers in the world entrusted with selectively breeding these sleek big cats, whose numbers are declining in their native ranges in Africa. It’s part of a worldwide conservation effort called the Species Survival Plan (SSP), a consortium of zoos, sanctuaries, and other expert advisors that manage animal pairings in order to maximize genetic diversity in populations of animals whose numbers are dwindling.
The day we visited, the cheetah keepers were frustrated. Two of the big cats who were perfect for each other—on paper—wanted nothing to do with romance. The male didn’t want to approach the female. The female didn’t want to approach the male. The chemistry wasn’t there. We’ve heard the same story from selective breeders of giant pandas, bustards, ferrets, hyenas, and a range of hoofstock: zero attraction between two potential mates, although both were of appropriate breeding age and experience. As one zoo biologist put it: “Things don’t always go well when a male and female first meet.”
Veterinarians have found that in agricultural animals, even what we might call “the mood” needs to be right. Severely inclement weather can inhibit sexual interest. For breeding stallions, turnoffs include a slippery floor or too many human spectators. For cows, who show more signs of arousal at night, time of day can be important.
Chemistry—the special attraction that individuals have for one another that contributes to the desire to mate—is frustrating to try to manufacture if your job is to increase the planet’s population of baby pandas or cheetahs. But as a creature with desire to give, searching for another creature with desire to give back, chemistry can be one of the most exciting parts of being alive.
The complex feelings of attraction and desire that make up chemistry can be at their most overwhelming and mysterious during wildhood. Like the neurobiology that shapes the perception of status, and the fear profiles that create animal defense mechanisms, the physical and behavioral infrastructure of courtship is common across groups, yet uniquely personalized to an individual adolescent. And it develops through experience.
Salt, of course, wouldn’t have the words to describe her feelings, but physically, biologically, the inputs would be similar to those of other animals. We have no idea who Salt’s first mate was, but one thing was likely: he and Salt had chemistry. He was possibly a Norwegian, Canadian, or Greenlander who had migrated every summer, like she had, a young calf swimming at his mother’s side back and forth between this Caribbean breeding area and the northern feeding grounds. He too had probably witnessed courtship among older whales throughout his life and been part of an adolescent or young adult group that traveled the Atlantic together for a few years, learning to feed, avoid predators, and socialize. Perhaps one day he was invited to join the men’s chorus, where he learned the old songs and composed a few of his own.
Salt heard the chorus and swam toward the males, listening. Once she was close enough, she bathed in the music, assessing the singers for accuracy and creativity, contemplating the attractiveness of these possible mates. Her presence at the breeding ground indicated an initial level of interest, but it didn’t commit her.
Perhaps Salt’s first mate sang with a particular lilt that caught her ear. Perhaps he held a note in a certain lovely way that gave her the impression he was a strong and deep diver. Maybe the krill he’d fed on all summer in Norway or Canada or Greenland gave him a quality she couldn’t quite define but that told her he was healthy and a good forager.
Whatever the combination of factors, Salt approached and, with a signal that humpback researchers still don’t completely understand, chose him as her primary “escort.” However she did it—some say it’s with a slap of her pectoral fin; others just call it a signal—she indicated her desire. Her chosen escort signaled back, and so the age-old process began.
What happens next in the humpback courtship ritual is thrilling for whale watchers. Judging by the excited reports of tourists and seasoned scientists alike, what’s known as a “rowdy group” or more scientifically as a “competitive group” is one of the planet’s most magnificent behavioral displays. Two whale-watch boat captains with dozens of years of experience running tours off the Silver Bank described it like this on their website:
A receptive female will first acquire a single primary suitor known as an “escort.” If another male whale believes he is a more suitable mate and imposes himself upon the pair with the intention of displacing the escort, he is known as a “challenger.” When there is more than one challenger it is the beginning of a rowdy group, with each male whale vying for the coveted position at the female’s side.
A typical rowdy group consists of 3–6 males but groups as large as two dozen or more whales can be seen on the Silver Bank. The female sets the pace and the competition can cover many miles and last for many hours as the males jockey for position. The competition can be very physical, with males pushing or ramming with their rostrums [a beaky protuberance on their snouts]; striking with the bony “anvil” on the bottom of their chin; using flukes and pectoral fins to strike each other; snapping jaws or vocalizing, performing peduncle throws [powerful tail splashes], lunges and breaches to intimidate; and even trying to hold each other underwater to impair breathing in order to tire the opponent. Injuries can result, typically heavy scratches caused by barnacles on the chin and fins . . . rubbed raw and bloody, or even the cartilaginous dorsal fin can be snapped off.
Tony Wu, an underwater photographer who has captured shots of Pacific humpback competitive groups, calls the display “all-out pec-slapping, bubble-blowing, body-slamming, tail-whacking, guttural snorting, full-contact chaos.” Another cameraman, Roger Munns, documented a Tongan humpback rowdy group for the BBC natural history series Life and described being in the center of it as “incredible . . . like standing in the middle of a motorway.”
Despite the rowdiness, even seeming violence, experts on whale courtship note that the female controls the pace. Consent is hers to offer, to demand, and to solicit from the males. Males indicate their interest by participating in the run. Any male who doesn’t consent presumably doesn’t take part in the competition.
Competitive group behavior can last many exhausting hours. It ends abruptly with the mating of the female and her chosen male. Although rowdy groups have been observed in whales all over the world, surprisingly, whale scientists have rarely seen the moment of intercourse, perhaps because it appears to happen in a quick thirty seconds.
In 2010, a photographer reported having witnessed humpback intercourse in a Pacific pair. Near Tonga, the photographer said he caught a rowdy group that ended in an epic clash between two giant bulls, while off to the side the female mated quietly and quickly (a news report called it “brief and tender”) with a smaller, younger male.
SEXUAL BEGINNERS
Wildlife biologists readily recognize sexual inexperience because it reveals itself in behaviors that are often exaggerated and poorly timed. Flirtation and mounting are clumsy and sometimes miss the mark. We heard from a range of animal experts that despite this, or maybe because of it, animals from penguins to horses are more tolerant of sexual unsophistication when both partners are inexperienced.
Even a creature as unremarkable as a moth has a first time. You might not have had many opportunities to think about moth virginity, but you may be interested to know that even these insects are no more expert at first-time sex than whales or humans. We know this because of an intriguing study that an entomologist-turned-librarian undertook in a Minnesota cornfield.
Shannon Farrell was studying courtship behavior in the Ostrinia nubilalis moth. Because she needed sexual beginners, she started her research with 252 virgin moths—individuals she had bred in her lab, separated by sex and kept apart to guarantee their inexperience. She wanted to see how they acted during their first sexual encounters. In particular, she wanted to observe whether courtship behaviors were patterned—exactly the same, and innate—or whether beginners had individual variations, personal moth embellishments. Ostrinia nubilalis moths, like many members of the moth and butterfly family, assess and return desire with surprisingly complex behaviors described rather lyrically by entomologists as “fanning,” “circling,” “bowing,” “kneeling,” and even “embracing.”
Farrell’s research was funded by the U.S. Department of Agriculture, which was less interested in the whimsy of moth courtship dances and more invested in learning how to stop them. Ostrinia nubilalis by another name is the dreaded European corn borer, responsible for devastating millions of dollars in crops every year. The USDA was searching for behavioral alternatives to chemical pest controls. They wanted Farrell to learn whether courtship could be interrupted, limiting the spread of moths by preventing them from reproducing.
Farrell found that adult moths with breeding experience are very regular in the way they express sexual receptivity and desire. They do follow specific patterns. The moth beginners, on the other hand, are all over the place. Their courtship behaviors vary hugely. With time and experience their movements became more streamlined. We can’t know whether these first-time moths experienced mamihlapinatapai (the desire to connect without the knowledge of how to initiate). But in Farrell’s experiments, the moths’ first attempts were full of fumblings and missteps. Signals were misunderstood or ignored, by both males and females. Mastering the multilayered harmonics of courtship was challenging for the sexually inexperienced moths. The same is true for human sexual beginners.
Whether mating partners are rainbow trout, anole lizards, bald eagles, or human beings, sexual intercourse follows essentially the same patterned behavior. What sets each species and each individual apart, what confers uniqueness and beauty on cultures and individuals, is not the sex act, but rather the special behaviors that allow two individuals to express desire and connect.
For every species on the planet, first sex can be blundering or sweet, exciting or embarrassing, intimate or intimidating. Of course, just because the sex act is a patterned behavior doesn’t make it any less scary—or exciting, or pleasurable—at first. For some, the emotions involved in going from sexual inexperience to experience are a line of demarcation between childhood and adult life, which can be a profound moment. Gaining sexual experience can create a separation between children and their parents. Something feels different—even when nothing else in the parent/child relationship has changed.
It’s impossible to say exactly what Salt’s first underwater mating was like, or, for that matter, her fourteenth, some thirty-five years later. Whether her first rowdy group ran long or short, whether it involved lots of males or just one or two, and which male she chose will all remain mysteries of the deep.
IT’S COMPLICATED
Once adolescent animals have embarked on the journey, the landscape that lies ahead is as unique to each individual as every other aspect of their growth. Experiences are diverse, and those experiences create personalized sexuality profiles the same way that fear experiences create customized internal armors. Some animals remain together for a period of time after mating, resting, nuzzling, and touching. Titi monkeys, found throughout South America, bond by intertwining their tails after mating. Whether animals do it just for a few moments, a season, or a lifetime, the behavior is called “pair bonding.”
“Maintenance of monogamous pair bonding,” as scientists call it when it’s repeated by the same two animals, struck us as an amusingly clinical phrase for the emotional labor that couples invest in the sometimes exciting, sometimes tedious task of remaining relevant to one another in long-term relationships. One of the most common questions about animal romance concerns monogamy: Do any animals besides humans mate for life?
The committed, decades-long marriage-type pair bonds seen in many human cultures and couples are indeed rare in the animal world. Few animals celebrate their species’ equivalents of golden wedding anniversaries. Some birds, like swans and some hawks, do appear to maintain lifetime monogamous pair bonds. Some animals stick to one partner for a single breeding season and find a new one the next year. But most animals are not monogamous, and many are what biologists call promiscuous.
One animal, a seahorse relative called a pipefish, is notable for the way it maintains pair bonds over a lifetime. Pipefish couples have a remarkable daily ritual called a greeting ceremony. Every morning, the two fish meet at the same place and go through a brief swimming routine that includes back-arching, horizontal parallel-swimming, and vertical up-and-down bobbing. After several minutes of this, the couple separates, and they have no more contact until the next morning’s greeting. They do the ceremony only with each other. And they do it even during the nonreproductive season, when they’re not breeding. Judith Goodenough, an animal behaviorist, writes: “[I]t is thought that its function is solely to maintain the bond with the partner in preparation for the breeding season.”
DNA paternity tests show that, unlike the monogamous pipefish, female humpbacks have many different sexual partners over the course of their lives. At the end of the 1979 season, Salt and her mate likely parted ways. Salt headed for the Stellwagen Bank with her kin. Her mate probably swam away with his group, back to Norway, Canada, Greenland, or wherever his summer feeding grounds were.
If they reencountered one another in some future season, they might mate again, or perhaps the spark would be gone. But the chemistry that attracted them that first time, and the experience they gained from courting one another, would inform their future pairings. Courtship, the ancient and planetwide guide through desire and uncertainty, had brought two individuals together across thousands of miles of open ocean.
And this behavioral marvel is shared by many creatures. Mastering courtship behaviors requires understanding one’s own sexual interest, expressing it, accurately assessing the interest of another, and, crucially, mutually learning how to coordinate and synchronize behaviors. These steps, practiced over and over in a young animal’s life, lead to what is essentially an agreement between two animals to come together sexually. This animal agreement correlates closely with our human behaviors around consent.