Sounds Wild and Broken

Part I

Origins

Primal sound and the ancient roots of hearing

At first, sound on Earth was only of stone, water, lightning, and wind.

An invitation: listen, and hear this primal Earth today. Wherever life's voices are hushed or absent we hear sounds largely unchanged since Earth cooled from its fiery start more than four billion years ago. Pressing against mountain peaks, wind yields a low and urgent roar, sometimes twisting into itself with a whip crack as it eddies. In deserts and ice fields, air hisses over sand and snow. On the ocean shore, waves slam and suck at pebbles, grit, and unyielding cliffs. Rain rattles and drums against rock and soil, and seethes into water. Rivers gurgle in their beds. Thunderstorms boom and the surface of the Earth echoes its reply. Sporadic tremors and eruptions of the underworld punctuate these voices of air and water, sounding with geologic growls and bellows.

These sounds are powered by the sun, gravity, and the heat of the Earth. Sun-warmed air stirs the wind. Waves rise as gales strafe the water. Solar rays lift vapor, then gravity tugs rain back to Earth. Rivers, too, flow under gravity's imperative. The ocean tides rise and fall from the pull of the moon. Tectonic plates slide over the hot liquid heart of the planet.

About three and a half billion years ago, sunlight found a new path to sound: life. Today all living voices, save for a few rock-eating bacteria, are animated by the sun. In the murmurs of cells and the voices of animals, we hear solar energy refracted into sound. Human language and music are part of this flow. We are acoustic conduits for plant-snared light as it escapes to air. Even the growl of machines is animated by the burn of long-buried sunlight.

The first living sounds came from bacteria that sent infinitesimally quiet murmurs, sighs, and purrs into their watery surroundings. Bacterial sounds are now discernible to us only with the most sensitive modern equipment. A microphone in a quiet laboratory can pick up sounds from colonies of Bacillus subtilis, a species of bacteria commonly found in soils and mammalian guts. Amplified, these vibrations sound like the hiss of steam escaping from a tight valve. When a loudspeaker plays similar sounds back into flasks of bacteria, the cells' growth rate surges, an effect whose biochemical mechanism is as yet unknown. We can also "hear" bacteria by balancing them on the tip of a microscopic arm. This bacteria-coated strut is so small that every shudder from their cell surfaces makes it quiver. A laser beam directed at the arm records and measures these motions. This procedure reveals that bacteria are in constant shimmering motion, producing tremulous sound waves. The crests and troughs of the waves-the extent of the cell's vibratory movement-are only about five nanometers, one-thousandth of the width of the bacterial cell, and half a million times smaller than the deflections in my vocal folds when I speak.

Cells make sound because they are in continuous motion. Their lives are sustained by thousands of inner streams and rhythms, each one tuned and shaped by cascades of chemical reactions and relationships. Given this dynamism, it is not surprising that vibrations emanate from their cell surfaces. Our inattention to these sounds is puzzling, especially now that technologies allow our human senses to extend into the bacterial realm. Only a couple of dozen scientific papers have so far examined sound in bacteria. Likewise, although we know that bacterial membranes are studded with proteins that detect physical movement-shear, stretch, touch-how these sensors function with sounds is unknown. Perhaps there is a cultural bias at play here. As biologists, we're immersed in visual diagrams. In my own training, not once was I asked to use my ears in a lab experiment. The sounds of cells exist not only on the edge of our perception, but of our imagination, shaped as it is by habits and preconceptions.

Do bacteria speak? Do they use sound to communicate with one another just as they use chemicals to send information from one cell to another? Given that communication among cells is one of the fundamental activities of bacteria, sound would at first seem a likely means of communication. Bacteria are social beings. They live in films and clusters that are so tightly woven that they are often invulnerable to chemical and physical attacks that easily kill solitary cells. Bacterial success depends on networked teamwork and, at the genetic and biochemical levels, bacteria are constantly exchanging molecules. But to date, there are no documented examples of sonic signaling among bacteria, although their increased growth rates when exposed to the sounds of their own kind may be a form of eavesdropping. Sonic communication may be ill-suited to bacterial societies. They live at a scale so tiny that molecules can zip from one cell to another in a fraction of a second. Bacteria use tens of thousands of molecules within their cells, an extensive, complex, and ready-made language. For them, chemical communication may be cheaper, faster, and more nuanced than sound waves.

Bacteria, and their look-alike cousins the Archaea, were the only life on Earth for about two billion years. Larger cells-amoebas, ciliates, and their kin-evolved about 1.5 billion years ago. These larger cells, the eukaryotes, later gave rise to plants, fungi, and animals. Single eukaryote cells, like bacteria, are full of trembling motion. They, too, are not known to communicate by sound. No yeast cell sings to its mate. No amoeba shouts warnings to its neighbors.

Life's quiet continued with the first animals. These ocean dwellers had bodies shaped like disks and pleated ribbons made of cells held together by strands of protein fiber. If we could hold them now, they'd feel like filmy seaweed, thin and rubbery. Their fossil remains are lodged in rocks about 575 million years old. Collectively, they are known as the Ediacaran fauna, named for the Australian hills where some of their number were unearthed.

The bodily simplicity of the Ediacaran animals obscures their pedigree, leaving no telltale marks to assign them to groups we'd recognize today. No segmented body armor like arthropods. No stiff column down their backs like fish. No mouths, guts, or organs. And almost certainly, no sound-making devices. There is no hint on these animals of any body part that could make a coherent scrape, pop, thump, or twang. Contemporary animals with more complex bodies but superficially similar body shapes-sponges, jellyfish, and sea fans-are also voiceless, suggesting that these first animal communities were quiet places. To the hum of bacteria and other single-celled creatures, evolution added only the sloshes and swirls of water around soft disk- and fanlike animals.

For three billion years, life was nearly silent, its sounds confined to the tremors of cell walls and the eddies around simple animals. But during those long, quiet years, evolution built a structure that would later transform the sounds of Earth. This innovation-a tiny wiggly hair on the cell membrane-helped cells to swim, steer, and gather food. This hair, known as a cilium, protrudes into the fluid around the cell. Many cells deploy multiple cilia, gaining extra swimming power from clusters or pelts of the beating hairs. How cilia evolved is not fully understood, but they may have started as extensions of the protein scaffolding within the cell. Any motion in the water is transmitted into the weave of living proteins in the core of the cilium and then back into the cell. This transmission became the foundation for life's awareness of sound waves. By changing electrical charges in the cells' membranes and molecules, cilia translated motions exterior to the cell into the chemical language of the cells' interiors. Today all animals use cilia to sense sonic vibrations around them, using either specialized hearing organs or cilia scattered on the skin and in the body.

The rich animal sounds that we live among today, including our own voices, are a twofold legacy of the origin of cilia 1.5 billion years ago. First, evolution created diversity of sensory experience through the many ways that cilia are deployed on cells and on animal bodies. Our human ears are just one way of listening. Second, long after sensitivity to vibrations in water first appeared, some animals discovered how to use sound to communicate with one another. The interplay of these two legacies-sonic sensation and expression-fed evolution's creativity. When we marvel at springtime birdsong, an infant discovering human speech, or the vigor of chorusing insects and frogs on a summer evening, we are immersed in the wondrous legacy of the ciliary hair.

Unity and Diversity

In the moment of our birth, we are dragged across four hundred million years of evolutionary time. We turn from aquatic creatures to dwellers of air and land. We gasp, sucking the alien gas into lungs previously filled with warm, salty ocean. Our eyes are pulled from the dim, reddish glow of the deep into jabbing brightness. The chill of evaporation slaps our drying skin.

No wonder we wail. No wonder we forget, burying the memory in the soil of the subconscious.

Our earliest and only experience of sound before birth was the hum and throb of an aquatic cocoon. Our mother's voice found us, as did the sounds of her surging blood, breath flowing in lungs, and churning digestion. Fainter were the sounds of the world beyond our mother, from places then unimaginable to our mostly unformed brains. High tones were attenuated by the enclosing walls of flesh and fluid, and so our first sonic experiences were low and often rhythmic as her body pulsed and moved.

In the womb, hearing develops gradually. Before twenty weeks, our world is silent. At about twenty-four weeks, hair cells start to signal through nerves running to rudimentary auditory centers in the partly developed brain stem. Cells tuned to low-frequency tones mature first, and so our hearing starts with bass throbs and murmurs. Six weeks later, furious growth and differentiation of tissues result in a frequency range of hearing similar to that of an adult. Sound flows from mother's fluids into ours, directly stimulating the nerve cells in the innermost part of our ears, unmediated by ear canals, drums, or middle ear bones.

All of this gone, in a moment.

Birth removes us from our watery surrounds, but our final aural transition to air happens hours later. The fatty vernix that swaddles us at birth lingers in the ear canal, muffling airborne sound for a few minutes or, for some, days. Soft tissues and fluid likewise recede over hours from the bones of the middle ear. When these vestiges of our fetal selves finally dissolve, our ear canals and middle ears are filled with the dry air that is our inheritance as terrestrial mammals.

Yet even in adulthood the hair cells of our inner ears are bathed with fluid. We keep a memory of the primal ocean and womb inside the coils of our inner ear. The rest of the ear's apparatus-pinnae, middle ear chamber, and bones-delivers sound to this watery core. There, deep inside, we listen as aquatic beings.



I lie belly-down on the wooden dock. The splintery boards toast me with the stored heat of the summertime Georgia sun. In my nose, the sulfurous, ripe aroma of salt marsh. The flowing water under the dock is turbid, a mud soup sweeping past on a falling tide. IÕm on Saint Catherines Island, a barrier island whose eastern shores face the Atlantic. Here, on the western side of the island, ten kilometers of salt marsh separate me from the flood-prone piney woods of the mainland. In the humid air, these woods are mere haze on the horizon. Salt marsh grasses, interrupted by narrow, twisting tidal creeks, cover the intervening distance. These grasses grow knee or waist high on all the mudflats, as thickly packed and as deep green as lush fields of young wheat.

The marshes seem monotone, their uniform verdure spiced only by snowy egrets stalking the creek edges and the pumping wing beats of glossy ibises passing overhead. But these are the most productive habitats known on Earth, capturing and turning into plant material more sunlight per hectare than the lushest of forests. Marsh grasses, algae, and plankton thrive in the happy confluence of fertile mud and strong sun. Such abundance supports a diverse animal community, especially of fish. More than seventy fish species live in these tidal marshes. Ocean-dwelling fish also swim here to spawn. Their larvae grow in the protection and plenty of the marshes, then catch a ride to adulthood on an outbound tide.

For all terrestrial vertebrate animals, rich salt water such as this was our original home, first as single-celled creatures, then as fish. About 90 percent of our ancestry was underwater. I clamp headphones over my ears and drop a hydrophone from the dock. I'm taking my ears back to where they came from.

The heavy capsule, a waterproof rubber and metal ball containing a microphone, sinks quickly, pulling the cable after it. I wedge a cable loop under my knee, holding the hydrophone above the creek bottom's mud and debris, about three meters down in the opaque water.

When I first release the hydrophone, all I hear is the high gurgle of streaming water. As it descends, the swirling sounds fall away. Suddenly I'm plunged into a pan of sizzling bacon fat. Sparkles surround me, a sonic shimmer. Every glistening fragment is a fleck of sunlit copper, warm and flashing. I've arrived in the acoustic domain of snapping shrimp.

This crackling is common in tropical and subtropical salt waters worldwide. Its sources are the hundreds of species of snapping shrimp that live in seagrass, mud, and reefs. Most of these animals are half the length of my finger or smaller, equipped with one hefty claw for snapping and a lighter one for grasping. I'm hearing a chorus of claws.

As the claw snaps shut, a plunger slams into a socket, shooting forward a jet of water. In the wake of this jet, water pressure drops, causing an air bubble to pop into existence, then collapse. This implosion sends a shockwave through the water, the snap that I'm hearing. The sound pulse lasts less than a tenth of a millisecond, but it is strong enough to kill any small crustacean, worm, or fish larva within three millimeters of the claw tip. Shrimp use the sound as a territorial signal and jousting weapon. As long as they keep a centimeter away from their neighbors, they can spar unharmed.

The combined racket of snapping shrimp is, in some tropical waters, loud enough to befuddle military sonar. In World War II, US submarines hid among the snapping shrimp beds off Japan. To this day, navy spies deploying hydrophones must work around the sonic haze of shrimp claws.