Sounds Wild and Broken, page 7
For a few large dinosaurs from the Cretaceous we can make more precise reconstructions. The head of the nine-meter-long herbivorous Parasaurolophus bore a long, backward-extending crest. The tubes of the nasal cavity looped within this crest, giving the vocal tract a length of over three meters. Like a head-mounted tuba, the crest amplified and projected low-frequency sounds produced by the larynx. The skulls of Parasaurolophus’s relatives, the hadrosaurs, also possess cavities, suggesting that low bugling sounds may have been common among these giants.
Living alligators and larger birds use their windpipes and air sacs in the neck as inflatable horns, broadcasting low-frequency sounds. Given the widespread use of this sound-making technique, it is likely that the birds’ close cousins, the extinct dinosaurs, made similar sounds. If so, alongside the subwoofers of hadrosaurs, other dinosaur species may have called with sounds like those of some modern birds that sing partly with air sacs: dove and pigeon coos, booming sounds like the basso profundo thump of modern bitterns, or the strangled belch of ruddy ducks.
The dinosaur sounds that we hear in films do not reliably evoke ancient sounds. They are built to evoke emotional responses in humans using manipulated recordings of modern animals. The roar of Tyrannosaurus rex is a slowed-down infant elephant trumpeting sound, merged in the studio with lion roars, whale blow-hole blasts, and crocodile rumbles. Gentoo penguins give voice to velociraptors.
And what of the mammals in this era? The mammals of the Jurassic and Cretaceous periods were formerly thought to be mousy creatures living in the shadows of the dinosaurs, precursors to the mammal diversity that bloomed after the nonavian dinosaurs went extinct. New fossil discoveries, especially from China, have overturned this view. Early mammalian evolution produced an explosion of ecological forms, species that resembled modern shrews, rats, water voles, moles, weasels, marmots, badgers, and even flying squirrels. Flowering plants were likely partly responsible for this explosion, albeit indirectly. A few early mammals fed on sap, seeds, and fruit, but many were insectivorous. The newly abundant and diverse insect fauna provided ready food for vertebrate animals swift enough to catch them. Good hearing helped. The evolution about 160 million years ago among early mammals of the three middle ear bones, followed by an elongated cochlea, opened a new perceptual world: the high-frequency rustles and songs of insect prey. We do not know what any of these early mammals sounded like. It is possible that they squeaked, purred, roared, barked, and bellowed, like modern mammals. Unlike other land vertebrates, mammals have a diaphragm, adding both fine control and force to the breath, and a band of muscle within the vocal folds, allowing more precise tuning of vibrations.
Listening to Cretaceous forests would be a disconcerting mix of familiarity and oddness. I imagine stepping into this world: Insect choruses like those of modern rain forests, a soundscape filled with cicadas and katydids and others. Frogs peep and trill from pond edges and the water holes in large trees. Squirrel-like mammals chatter and grunt. Large herbivorous dinosaurs groan like subwoofers. Others hoot and trumpet like modern primates. Birds hop among the trees, gleaning insects and plucking fruit, as they do today. One of the birds opens its beak, revealing rows of sharp teeth. Instead of sweet whistles or ornamented trills, the feathered animal looses a sibilant cry or harsh grunt. At dawn, no surge of birdsong meets the rising sun. The melodies that birds today stitch into the air are absent from this Cretaceous soundscape.
The great explosion of sonic expression in the Cretaceous was rooted in the ecological and evolution revolution brought about by the flowering plants. For many animals, the catalyzing effect was direct: flowering plants nourished animals and then co-evolved with them as pollinators, herbivores, and fruit dispersers. For other species, the boost was indirect, largely through the new varieties and abundance of insect foods made possible by flowering plants. If flowering plants had not evolved, if the land’s food web was still entirely based on ferns and conifers, the world would sound less diverse and less exuberant. Many of our most familiar singers—katydids, cicadas, birds, and others—would either not exist as songsters or be muted and monotone.
In our present biodiversity crisis, this history offers a warning. We cannot destroy botanical diversity without also silencing the animals that give voice to the living Earth. Ninety percent of the half million plant species on Earth are flowering plants. Although we lack population data on most species, the current best estimate is that at least 20 percent of the world’s plant species are threatened with extinction.
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There are two significant exceptions to the tight association between floral diversity and the expansion of sonic expression. One is in the sounds of the oceans. The other is in the words you read on this page, the human voice captured in ink.
In 1956, when French explorer and filmmaker Jacques-Yves Cousteau released one of the first color documentaries about the ocean, a film that received both the Cannes Film Festival Palme D’Or and a US Academy Award, he called the work Le Monde du Silence, the world of silence. But the oceans are not silent. Human physiology was the first barrier to listening in the sea. Inattention was the second.
Our ears are adapted to air, not water. Submerged, we can only hear a few loud sounds. And so the aquatic world’s many sonic textures and nuances are mostly lost on our unaided ears. Although hydrophone technologies were developed in the early twentieth century, they were deployed mostly by the military for listening to shipping and submarines. Adding to the problem, before the 1960s biologists mostly studied the ocean by killing or otherwise silencing their subjects. In Cousteau’s film, lobsters are tugged from their holes, fish hauled on board, sharks slaughtered, and coral reefs dynamited, methods that reflect the crude scientific tools of the time. Early scuba explorations brought scientists into more intimate and less destructive contact with sea life, but listening was hampered by the constant drone of boat noise and the roar of bubbles streaming over divers’ ears.
We now know that the oceans are full of sound. Biologists and sound recordists, including later work by Cousteau and his team, have deployed hydrophones from the Arctic to the tropical coral reefs, finding waters alive, always, with sound. A pioneer in this work was Marie Poland Fish, a biologist at the University of Rhode Island, whose navy-supported studies of underwater sounds, starting in the 1940s, revealed “sea sounds and languages” among fish and crustaceans. She wrote, in the same year that Cousteau released his film, that “the din of animal life pervades the underwater world as it does our forests, countryside and cities.” We now know that, far from being silent, waters crackle and glow with choruses of snapping shrimp and other crustaceans. Fish, sometimes gathered by the tens of thousands on their breeding grounds, drum, twang, and purr. Marine mammals—seals, sea lions, walruses, dolphins, whales—click, boing, moan, and ring like bells. These sounds of life combine with the seethe of wind-stirred froth, the boom of colliding waves, and the groan and crack of ice sheets. Sound in water travels fast and far. Unlike on land, its energies flow unimpeded into animal bodies. Sound in oceans is ubiquitous and deeply felt by its creatures.
As was true on land, these sonic marvels of animals came late in evolution. Even after trilobites, fishes, and other complex animals evolved, communicative sound was absent, or so it presently seems from the fossil record. Toothed jaws clicked, fins swished, and body armors grated and snapped. Most sea creatures could hear, both finding food and avoiding predation by eavesdropping on the sonic clues evoked by the motions of other creatures. But in ancient oceans, no known animals called out to mates, cried warnings at predators, or whispered to offspring.
The first ocean creatures to break the long communicative silence that marked the first 300 million years of animal evolution were likely the spiny lobsters. Recognizable today by their long, often prickly antennae and lack of large front claws, these distant relatives of “true” lobsters live in warm waters worldwide. They can grow to over a meter in length and are an important human food source, with an annual global catch of over eighty thousand metric tons. Next time you see one staring dead-eyed from a pile of ice chips in the supermarket, take a close look at the details of the face: you are in the presence of the ocean’s earliest known communicative sound. A nub on the base of the antenna rubs against a smooth track running down from the eye. In life, this makes a yelping sound loud enough to scare away predatory fish or crustaceans. Today, in productive habitats such as the coasts of Japan and Western Europe, a hydrophone can detect dozens of spiny lobster calls per hour and the sounds of the largest animals can reach up to three kilometers.
The spiny lobster makes its defensive squeal with a unique sound-producing mechanism. Although the nub and track seem smooth, their microscopic structures create a “stick-and-slip” motion as the rubbery nub slides over a sheet of microscopic shingles on the track. As the antenna slides toward the eye, the nub jerks forward, sticks, then repeats, creating a juddering motion and a sound wave. A violin bow acting on a string works the same way. Its motion seems fluid, but the rosin-covered horsehair of the bow goes through a rapid series of sticks and slips as it moves over the string, a jerky motion that drives the string into vibration.
The nub and shingled track can squeak even when the spiny lobsters’ skeletons are soft after molting, the most vulnerable time in the life cycle of most crustaceans. Sound therefore not only gives these animals a defense mechanism, startling potential predators, it protects them when their other defenses are down.
Evolutionary family trees reconstructed from DNA sequences suggest that spiny lobsters first evolved in the Jurassic, about 220 million years ago, followed by diversification from 200 to 160 million years ago. The first definitive fossil specimens are 100 million years old.
Fossil evidence suggests that other sound-making crustaceans evolved after the spiny lobsters, around 95 to 70 million years ago. Crabs and lobsters with ridges along their thorax and claws first appeared at this time, and these structures were similar to those used by living animals to purr and growl. Like those of the spiny lobsters, these sounds are used as defenses against attacks, but some species also use them as mating or territorial displays.
The timing of the origin of snapping shrimp sounds—one of the loudest and most widespread animal sounds in the oceans—is uncertain. Genetic evidence suggests that the group may have split from other crustaceans in the Jurassic, 148 million years ago. But, the first fossil evidence of a claw that snaps dates to less than 30 million years ago, and much of the modern diversity of the group is less than 10 million years old. It seems likely, then, that although these animals or their ancestors may have been present in the Jurassic, their sparkling clouds of sound appeared much later.
One thousand species of modern fish are known to make sounds. This is likely a vast underestimate given that most fish species have yet to be studied in any detail. The known mechanisms of sound production are diverse, reflecting at least thirty different evolutionary inventions across the fish family tree. Catfish, piranhas, squirrelfish, and drums use high-speed muscles attached on and near the swim bladder to evoke purrs, taps, or squeaks from the gas-filled chamber. Butterflyfish and cichlids vibrate their ribs and limb girdles, causing the swim bladder to vibrate. Seahorses click their head and neck bones. Damselfish slam their teeth so hard that their swim bladders croak. Grinding teeth supplement the swim-bladder cries of grunts. Catfish strum their pectoral fins.
These are modern groups of fishes, evolved in the last 100 million years. It is possible that fishes were calling out to one another with their swim bladders long before this time, but the thin-walled bladder and its muscles do not fossilize, and leave no evidence. Bichir and sturgeon, living descendants of lineages that split from other fish 350 million years ago, make knocks, moans, and rumbling sounds when they are close to others or spawning. Perhaps their ancestors did, too, although it is also possible that their sound making evolved during the hundreds of millions of years after the lineages split. The sounds of fish in deep time are hard to discern. We can, though, conclude that the many fish voices that now animate waters worldwide come almost entirely from groups of recent origin.
It seems that for hundreds of millions of years, the fish, crustaceans, and other animals of the oceans made few, if any, communicative sounds. Then, starting around two hundred million years ago and accelerating around one hundred million years ago, most of the voices of the ocean arrived.
Three factors seem to have driven the rise of sonic diversity in the oceans: the breakup of a supercontinent, a hothouse climate, and a sexual revolution.
Starting 180 million years ago, the supercontinent Pangaea fragmented, a process that continued for another 120 million years. These fractures created the major continents and oceans as we know them today. New shorelines and coastal habitats opened worldwide, increasing the extent and diversity of ocean habitat and opening new opportunities for colonization and adaptation. The sound-making animals of the seas diversified during this time when new oceanic habitats were expanding.
A long period of greenhouse climate also increased sonic diversity. Temperatures were so hot during most of the Cretaceous that ocean waters were tropical almost from pole to pole. There were no permanent ice sheets, and the sea level was up to two hundred meters higher than it is today, further broadening marine habitat as Pangaea broke up. North America was bisected by a large sea. Most of northern Europe and North Africa were underwater. Life abounded in these spacious and hospitable waters. Photosynthetic plankton, the base of the ocean food web, was abundant and evolved a burst of new forms. Fish, crustaceans, snails, and echinoderms also multiplied. The sound-making animals that evolved and diversified during this time were almost all predators, most of them also formidably defended by tough skeletons or speedy bodies: spiny lobsters, lobsters, snapping shrimp, and fish. Sound making was a luxury enjoyed only by those at the top of a rich food chain. Prey animals at this time stayed silent and evolved thicker shells, and many took to living buried in mud and sand.
Mating behaviors also seem to have driven the origins and diversification of sound-making ocean animals. Many sea creatures, unlike any land animal, shed sperm and eggs into the water without ever coming near another member of their own species. Clams, many snails, corals, and others breed without intimate contact. These species are also generally silent. With no nearby mates, why sing? During the breakup of Pangaea, species that bred this way showed no increase in diversity. But animals that breed by coming into close physical contact, rubbing bodies together or grasping one another, tripled in diversity during this time. These animals often make sounds to attract mates or repel sexual rivals. Crabs and lobsters both woo partners and spar with rivals by stridulating their exoskeletons. The diverse arrays of thumps, squeaks, growls, and pulsed tones among fish are mostly breeding signals.
Why should intimate mating behaviors increase species diversity? Animals that breed by copulating do so only with mates that live nearby. This keeps gene exchange local, allowing species to break into regional variants and, eventually, new species. But species that broadcast eggs and sperm in water currents have widespread and homogenous gene pools. They are like large, monolithic human corporations. These giants may be good at what they do, but they cannot break into specialized, innovative subgroups. Species with behaviors that enforce local mating are more like swarms of start-up companies, each one able to pursue its own regional opportunities without being swamped by gene flow from far away. This likely yielded many new species during the time when Pangaea’s breakup created new habitats.
There is one significant group of latecomers to the sonic blossoming of the seas: whales, seals, and other marine mammals. In a deliciously convoluted evolutionary path, the structure that stopped water flowing into the lungs of the lungfish and first land vertebrates, the larynx, returned to the water and sang. By blocking their blowholes or nostrils, these marine mammals use the vibrations of vocal folds in their larynx to send sounds through their body tissues and out into the water. Among the toothed whales, the larynx is supplemented by whistling air sacs and a sound-focusing “melon” in the forehead, sending focused beams of sound forward, like a sonic headlamp. When a solid object reflects the beam, the whale uses the echoes to home in on prey, avoid obstacles, or “see” its companions. Because sound penetrates tissues, this echolocating vision also reveals the inner form of other creatures. Sound, for toothed whales, gives a living MRI scan of the surrounding world.
Whales descend from pig- or deerlike ungulates, and their transition from land to water took ten million years, starting fifty million years ago. Seals and their kin are carnivores and arrived in the water later, twenty million years ago. The teeth and limbs of the transitional ancestors suggest that both groups were drawn to the water in search of the abundant food in nearshore habitats, just as polar bears and sea otters today spend much of their time foraging in the water or at its edge.
To the creative forces of climate, biogeography, and mating that brought forth the sounds of fish and crustaceans, we can add the later opportunistic colonization of the seas by hungry mammals. The hot blood, large brains, specialized teeth, and communicative vocal networks of these pioneers—all qualities that first evolved on land—gave them an advantage when they turned their attention to the seas. We hear the result in whale cries loud enough to traverse entire ocean basins or in the squealing of seals where fish abound in nearshore habitats.

