FOUR

What a Plant Hears

The temple bell stops but I still hear the sound coming out of the flowers.

—Matsuo Basho

Forests reverberate with sounds. Birds sing, frogs croak, crickets chirp, leaves rustle in the wind. This never-ending orchestra includes sounds that signal danger, sounds related to mating rituals, sounds that threaten, sounds that appease. A squirrel jumps on a tree at the crunch of a breaking branch; a bird answers the call of another. Animals constantly move in response to sound, and as they move, they create new sounds, contributing to a cyclical cacophony. But even as the forest chatters and crackles, plants remain ever stoic, unresponsive to the din around them. Are plants deaf to the clamor of a forest? Or are we just blind to their response?

While various forms of rigorous scientific research have helped shed light on the plant senses we’ve covered so far, little credible, conclusive research exists when it comes to a plant’s response to sound. This is surprising, given the amount of anecdotal information we have about the ways in which music may influence how a plant grows. While we may think twice when we hear that plants can smell, the idea that plants can hear comes as no surprise at all. Many of us have heard stories about plants flourishing in rooms with classical music (though some people claim it’s really pop music that gets a plant moving). Typically, though, much of the research on music and plants has been carried out by elementary school students and amateur investigators who do not necessarily adhere to the controls found in laboratories grounded in the scientific method.

Before we delve into whether or not plants can actually hear, let’s get a better understanding of human hearing. A common definition of “hearing” is “the ability to perceive sound by detecting vibrations via an organ such as the ear.” Sound is a continuum of pressure waves that propagate through the air, through water, or even through solid objects such as a door or the earth. These pressure waves are initiated by striking something (such as by beating a drum) or starting a repeated vibration (like plucking a string) that causes the air to compress in a rhythmic fashion. We sense these waves of air pressure through a particular form of mechanoreception by tactile-sensitive hair cells in our inner ears. These hair cells are specialized mechanosensory nerves from which extend hairlike filaments called stereocilia that bend when an air-pressure wave (a sound) hits them.

The hair cells in our ears convey two types of information: volume and pitch. Volume (in other words, the strength of the sound) is determined by the height of the wave reaching the ear, or what’s better known as the amplitude of the waves. Loud noises have high amplitude, and soft noises have low amplitude. The higher the amplitude, the more the stereocilia bend. Pitch, on the other hand, is a function of the frequency of the pressure waves—how many times per second the wave is detected regardless of its amplitude. The faster the frequency of the wave, the faster the stereocilia bend back and forth and the higher the pitch.*

(* Sound waves are measured in hertz (Hz), where 1 Hz equals one wave cycle per second. We can hear sound waves in the range of 20 Hz for low pitches to up to 20,000 Hz for the highest pitches. The lowest note on a contrabass, for example (the low E), vibrates at 41.2 Hz, while the highest note on a violin (high E) vibrates at 2,637 Hz. The highest C on a piano vibrates at 4,186 Hz, and the C two octaves above this vibrates at about 16,000 Hz. A dog’s ear responds to sound waves above 20,000 Hz (which is why we can’t hear dog whistles), and bats even emit and detect rebounding sound waves up to 100,000 Hz for their internal sonar that maps out the landscape ahead of them. At the other end of the spectrum, an elephant can hear and vocalize sounds below 20 Hz, which human beings also can’t detect.)

As the stereocilia vibrate in the hair cells, they initiate action potentials (as do other types of mechanoreceptors that we encountered in the previous chapter) that are relayed to the auditory nerve, and from there they travel to the brain, which translates this information into different sounds. So human hearing is the result of two anatomical occurrences: the hair cells in our ears receive the sound waves, and our brain processes this information so that we can respond to different sounds. Now, if plants are capable of detecting light without having eyes, can they detect sound if they don’t have ears?

Rock-and-Roll Botany

At one point or another, many of us have been intrigued by the idea that plants respond to music. Even Charles Darwin (who, as we’ve seen, carried out his seminal research into plant vision and feeling over a century ago) studied whether plants could pick up on the tunes he played for them. In one of his more bizarre experiments, Darwin (who, in addition to his lifetime commitment to biology research, was an avid bassoonist) monitored the effects of his own bassoon music on plant growth by seeing if his bassoon could induce the leaves of the Mimosa plant to close (it couldn’t, and he described his study as a “fool’s experiment”).

Research dealing with plant auditory prowess hasn’t exactly blossomed since Darwin’s failed attempts. Hundreds of scientific articles have been published in the last year alone that deal with plant responses to light, smell, and touch, yet only a handful have been published over the last twenty years that have dealt specifically with plant responses to sound, and even then many of them don’t hold up to my standards for what would be evidence of a “hearing” plant.

An example of one of these papers (albeit a zany one) was published in The Journal of Alternative and Complementary Medicine. It was written by Gary Schwartz, a professor of psychology and medicine, and his colleague Katherine Creath, a professor of optical sciences, both based at the University of Arizona, where Schwartz founded the VERITAS Research Program. This program “test[s] the hypothesis that the consciousness (or personality or identity) of a person survives physical death.” Obviously, studying consciousness after death presents some experimental difficulties, so Schwartz also studies the existence of “healing energy.” Because human participants in a study can be strongly influenced by the power of suggestion, Schwartz and Creath used plants instead, in order to uncover the “biologic effects of music, noise, and healing energy.” Of course, plants cannot be influenced by the placebo effect or, as far as we know, by musical preferences (though researchers carrying out and analyzing experiments can be).

They hypothesized that healing energy and “gentle” music (which consisted of Native American flute and nature sounds, which they noted were preferred by the experimenter) would be conducive to the germination of seeds.* Creath and Schwartz explained that their data revealed that slightly more zucchini and okra seeds germinated in the presence of gentle music sounds than seeds that were kept in silence. They also noted that germination rates could increase as a result of Creath’s healing energy, which she applied to the seeds with her hands.** It goes without saying that these results have not been validated by subsequent research in other plant laboratories, but one of the sources Creath and Schwartz cited in support of their results was Dorothy Retallack’s The Sound of Music and Plants.

(* It’s interesting that they chose “gentle” sounds as they cite Pearl Weinberger from the University of Ottowa, who used ultrasonic waves (which are definitely not gentle) in her studies in the 1960s and 1970s.)

(** Creath was trained in VortexHealing, which is described as “a Divine healing art and path for awakening. It is designed to transform the roots of emotional consciousness, heal the physical body, and awaken freedom within the human heart. This is the Merlin lineage.” See www.vortexhealing.com.)

Dorothy Retallack was a self-described “doctor’s wife, housekeeper and grandmother to fifteen,” and she enrolled as a freshman in 1964 in the now-defunct Temple Buell College after her last child had graduated from college. Retallack, a professional mezzo-soprano who often performed at synagogues, churches, and funeral homes, decided to major in music at Temple Buell. She took an Introduction to Biology course to complete her science requirements and was asked by her teacher to carry out any experiment that she thought would interest her. Retallack’s juxtaposing of her biology requirement with her love for music resulted in a book spurned by mainstream science but quickly embraced by the popular culture.

Retallack’s The Sound of Music and Plants provides a window into the cultural-political climate of the 1960s, but it also sheds light on her perspective as well. Retallack comes across as a unique mixture of a social conservative who believed that loud rock music correlated with antisocial behavior among college students and a New Age religious spiritualist who saw a sacred harmony between music and physics and all of nature.

Retallack explained that she was intrigued by a book published in 1959 titled The Power of Prayer on Plants, in which the author claimed that plants that were prayed to thrived while those bombarded with hateful thoughts died. Retallack wondered whether similar effects could be induced by positive or negative genres of music (the ruling of positive or negative was dictated, of course, by her own musical taste). This question became the basis of her research requirement. By monitoring the effect of different music genres on plant growth, she hoped to provide her contemporaries with proof that rock music was potentially harmful—not only to plants, but to humans as well.

Retallack exposed different plants (philodendrons, corn, geraniums, and violets, to name a few—each experiment used a different species) to an eclectic collection of recordings, including music by Bach, Schoenberg, Jimi Hendrix, and Led Zeppelin, and then monitored their growth. She reported that the plants exposed to soft classical music thrived (even when she exposed them to Muzak, that sublime elevator music we all know and love) while those exposed to Led Zeppelin II or Hendrix’s Band of Gypsys were stunted in their growth. To show that it was in fact the drumbeats of the likes of the legendary drummers John Bonham and Mitch Mitchell that were harming the plants, Retallack repeated her experiments using recordings of the same albums but with the percussion blocked out.

As she hypothesized, the plants were not as damaged as they had been when they were blasted with the full versions, drums included, of “Whole Lotta Love” and “Machine Gun.” Could this mean that plants have a preferred musical taste that overlapped with Retallack’s? And on a worrisome note, as someone who grew up studying with Zeppelin and Hendrix blaring from my stereo system at all times, I wondered when I first encountered this book if these results implied that I too could have been damaged, as Retallack extrapolates from her results to the effect of rock music on young people.

Dorothy Retallack in the lab with her adviser Dr. Francis Broman

Fortunately for me and for the hordes of other Zeppelin fans out there, Retallack’s studies were fraught with scientific shortcomings. For example, each experiment included only a small number of plants (fewer than five). The number of replicates in her studies was so small that it was not sufficient for statistical analysis. The experimental design was poor—some of the studies were carried out in her friend’s house—and parameters, such as soil moisture, were determined by touching the soil with a finger. While Retallack cites a number of experts in her book, almost none of them are biologists. They are experts in music, physics, and theology, and quite a few citations are from sources with no scientific credentials. Most important, however, is the fact that her research has not been replicated in a credible lab.

In contrast to Ian Baldwin’s initial studies on plant communication and volatile chemicals (encountered in chapter two), which were originally met with resistance by the mainstream science community but subsequently validated in many labs, Retallack’s musical plants have been relegated to the garbage bin of science. While her findings were reported in a newspaper article, attempts to publish her results in a reputable scientific journal were unsuccessful, and her book was eventually published as New Age literature. This of course hasn’t stopped the book from becoming part of the cultural zeitgeist.

Retallack’s results also contradicted an important study published in 1965. Richard Klein and Pamela Edsall, scientists from the New York Botanical Garden, decided to run several tests to determine if plants were truly affected by music. They did this in response to studies coming out of India claiming that music increased the number of branches that would sprout in different plants, one of which was the marigold (Tagetes erecta). In an attempt to recapitulate these studies, Klein and Edsall exposed marigolds to Gregorian chant, Mozart’s Symphony no. 41 in C major, “Three to Get Ready” by Dave Brubeck, “The Stripper” by the David Rose Orchestra, and the Beatles’ songs “I Want to Hold Your Hand” and “I Saw Her Standing There.”

Klein and Edsall concluded from their study (which employed strict scientific controls) that music did not influence the growth of the marigolds. As they reported, using humor to convey their general indignation at this line of research, “There was no leaf abscission traceable to the influence of ‘The Stripper’ nor could we observe any stem nutation in plants exposed to The Beatles.”* How can we explain the contradiction between these results and Retallack’s subsequent studies? Either Klein and Edsall’s marigolds had different musical taste from Retallack’s plants, or, more likely, the major methodological and scientific discrepancies in Retallack’s study led to unreliable results.

(* Nutation is the cyclical swaying or bending movement displayed by different plant parts.)

While Klein and Edsall’s research was published in a respected professional science journal, it was basically unseen by the general public, and research like Retallack’s continued to dominate the popular press in the 1970s. It is also featured prominently in Peter Tompkins and Christopher Bird’s iconic book from 1973, The Secret Life of Plants, which was marketed as a “fascinating account of the physical, emotional, and spiritual relations between plants and man.” In a very lively and beautifully written chapter titled “The Harmonic Life of Plants,” the authors reported that not only do plants respond positively to Bach and Mozart but they actually have a marked preference for the Indian sitar music of Ravi Shankar.* Much of the science featured in The Secret Life of Plants relied on subjective impressions based on only a small number of test plants. The renowned plant physiologist, professor, and known skeptic Arthur Galston put it succinctly when he wrote in 1974: “The trouble with The Secret Life of Plants is that it consists almost exclusively of bizarre claims presented without adequate supporting evidence.” But this hasn’t kept The Secret Life of Plants from influencing modern culture either.

(* Some of the shortcomings of Retallack’s research are also pointed out in The Secret Life of Plants.)

Marigold (Tagetes erecta)

More recent data supporting any significant plant response to sound are lacking. However, careful examination of the scientific literature reveals results peppered throughout articles reporting other findings that debunk the idea that plants can hear. In Janet Braam’s original paper on the identification of the TCH genes (the genes that were activated upon touching a plant), she explained that she checked if in addition to physical stimulation, these genes were induced by exposure to loud music (which for her was provided by Talking Heads). Alas, they were not. Similarly, in Physiology and Behaviour of Plants, the researcher Peter Scott reported a series of experiments that were set up to test whether corn is influenced by music, specifically Mozart’s Symphonie Concertante and Meat Loaf’s Bat Out of Hell. (It’s amazing what these types of experiments can tell us about a scientist’s own musical taste.) In the first experiment, the seeds exposed to Mozart or Meat Loaf germinated more rapidly than those left in silence. This would be a boon to those who have claimed that music affects plants and a bane to those who think Mozart is qualitatively better than Meat Loaf.

But this is where the importance of proper experimental controls comes into play. The experiment continued, but this time a small fan circulated any heated air from the speakers away from the seeds. In this new set of experiments, there was no difference in germination rates between the seeds left in silence and those exposed to music. The scientists discovered in the first set of experiments that the speakers playing the music had apparently radiated heat, which improved germination efficiency; the heat was the determining factor, not Mozart’s or Meat Loaf’s music.

Keeping a skeptic’s view, let’s look again at Retallack’s conclusion that the intense drumbeats of rock music are detrimental to plants (and also to people). Could there be an alternative, scientifically valid explanation for loud drumming having a negative effect on plants? Indeed, as I highlighted in the previous chapter, both Janet Braam and Frank Salisbury clearly showed that simply touching a plant a number of times led to dwarfed, stunted plants, or even to a plant’s death. So it is conceivable that heavy rock percussion, if pumped through the proper speakers, leads to such powerful sound waves that plants vibrate and are literally “rocked” back and forth as if in a windstorm. In such a scenario we would expect to find reduced growth in plants exposed to Zeppelin, as is the case reported by Retallack. Maybe it’s not that the plants don’t like rock music; maybe they just don’t like being rocked.

Alas, until it is proven otherwise, it looks as if all evidence tells us that plants are indeed “deaf,” which is interesting if you consider that plants contain some of the same genes known to cause deafness in humans.

Deaf Genes

T

Corn (Zea mays)

he year 2000 was a hallmark for the plant sciences. It was the year that the sequence of the entire Arabidopsis thaliana genome was finally communicated to scientists around the world, and they were all eager to hear the results. More than three hundred researchers based at universities and biotechnology companies worked over four years to determine the order of approximately 120 million nucleotides that make up the DNA of the arabidopsis. It also cost approximately seventy million dollars. (The money and the collective effort associated with this project are unfathomable today, as technology has progressed to the point where a single lab can sequence an arabidopsis genome in a little over a week for less than 1 percent of the original cost.)

Arabidopsis was chosen by the National Science Foundation back in 1990 as the first plant that would have its genome sequenced thanks to an evolutionary quirk that resulted in its having relatively little DNA compared to other plants. While arabidopsis has almost the same number of genes (twenty-five thousand) as most plants and animals, it contains very little of a type of DNA called noncoding DNA, which made determining its sequence relatively easy to do. Noncoding DNA is found all over the genome, separating between genes, at the ends of chromosomes, and even within genes. To put things in perspective: while arabidopsis contains about twenty-five thousand genes in 120 million nucleotides, wheat has the same number of genes in 16 billion nucleotides (and human beings have about twenty-two thousand genes, fewer than the petite arabidopsis, in 2.9 billion nucleotides).* Because of its small genome, small size, and fast generation time, arabidopsis became the most widely studied plant in the late twentieth century, and as a result, research on this common weed has led to important breakthroughs in many fields. Almost all of the twenty-five thousand genes found in arabidopsis are also present in plants that are important agriculturally and economically, such as cotton and potato. This means that any gene identified in arabidopsis (say, a gene for resistance to a particular plant-attacking bacteria) could then be engineered into a crop to improve its yield.

(* These numbers should be taken with a grain of salt as the precise definition of “gene” is evolving and with it the numbers. But the general trends and scales are correct.)

The sequencing of the arabidopsis and human genomes led to many surprising findings. Most relevant to our discussion here is that the arabidopsis genome was found to contain more than a few genes known to be involved in diseases and disabilities in humans. (The human genome, on the other hand, contains several genes known to be involved in plant development, such as a group of genes called the COP9 signalosome that mediate plant responses to light.) As scientists deciphered the arabidopsis DNA sequence, they discovered that the genome contains the BRCA genes (which are involved in hereditary breast cancer), CFTR (which is responsible for cystic fibrosis), and a number of genes involved in hearing impairments.

An important distinction must be made: while genes are often named for diseases associated with them, the gene doesn’t exist to cause the disease or impairment. A disease occurs when the gene doesn’t function properly as a result of a mutation, which is a change in the sequence of nucleotides that builds the gene that disrupts the DNA code. To refresh our understanding of basic human biology: our DNA code is comprised of only four different nucleotides, which are abbreviated A, T, C, and G. The specific combination of these nucleotides provides the code for different proteins. A mutation or a deletion of a few nucleotides can catastrophically alter the code. The BRCA are genes that, when mutated or disrupted, can cause breast cancer, but under normal circumstances they play a key role in determining how cells know when to divide. When the BRCA genes don’t function normally, cells divide too often, and this can lead to cancer. CFTR is a gene that, when mutated, when disrupted, causes cystic fibrosis but normally regulates the transport of chloride ions across the cell membrane. When this protein doesn’t work properly, chloride ion transport in the lungs (and other organs) is blocked, leading to the accumulation of thick mucus, which manifests clinically as a respiratory ailment.

The names of these genes have nothing to do with their biological functions, only their clinical outcome. What are these genes doing in green plants? The arabidopsis genome contains BRCA, CFTR, and several hundred other genes associated with human disease or impairment because they are essential for basic cellular biology. These important genes had already evolved some 1.5 billion years ago in the single-celled organism that was the common evolutionary ancestor to both plants and animals. Of course, mutations in the arabidopsis versions of these human “disease genes” also disrupt the way the plant functions. For example, mutations in the arabidopsis breast cancer genes lead to a plant whose stem cells (yes, arabidopsis has stem cells) divide more than normal cells, and the whole plant is hypersensitive to radiation, both of which are also hallmarks of human cancer.

This puts in perspective what a “deaf” gene is: a gene that—when mutated—leads to deafness in humans. More than fifty human “deaf” genes have been identified by various labs worldwide, and at least ten of these fifty also show up in arabidopsis. Just because deaf genes were discovered in the arabidopsis genome doesn’t mean that the plant can hear, just as the presence of BRCA in arabidopsis doesn’t mean plants have breasts. The human “deaf” genes have a cellular function necessary for the ear to work properly, and when any of these genes contain a mutation, the result is hearing loss.

Four of the arabidopsis genes connected to hearing impairment encode very similar proteins called myosins. Myosins are known as motor proteins, because they work as “nanomotors” that literally carry and move different proteins and organelles around the cell.* One of the myosins involved in hearing helps form the hair cells in the inner ear. When this myosin contains a mutation, our hair cells don’t form properly, and they don’t respond to sound waves. In the plant world, we find that plants have hairlike appendages on their roots, aptly referred to as root hairs which help roots soak up water and minerals from the soil. When a mutation occurs in one of the four arabidopsis “deaf” myosin genes, the root hairs don’t elongate properly, and consequently the plants are less efficient at absorbing water from the soil.

(* This website illustrates myosin in action: www.sci.sdsu.edu/movies/actin_myosin_gif.html.)

Myosin and the other genes found in both plants and humans have similar functions at the cellular level. But when you put all the cells together, the function for the particular organism is different: we need myosin to facilitate the proper functioning of our inner-ear hairs and, ultimately, to hear; plants need myosin for the proper functioning of their root hairs, which allows them to drink water and find nutrients from the soil.

The Deaf Plant

Serious and reputable scientific studies have concluded that the sounds of music are truly irrelevant to a plant. But are there sounds that, at least theoretically, could be advantageous for a plant to respond to? Professor Stefano Mancuso, director of the International Laboratory of Plant Neurobiology at the University of Florence, has recently been using sound waves to increase yield in a vineyard in the Tuscany wine region. But the basic biology behind this agricultural use of sound waves is still unclear.

Dr. Lilach Hadany, a theoretical biologist at Tel Aviv University, uses mathematical models to study evolution. She proposes that plants do respond to sounds but that we have yet to carry out the correct experiments to detect their doing so. Indeed in science in general, lack of experimental evidence does not equate to a negative conclusion. In her mind, we would have to construct a study in which we would use a sound from the natural world known to influence a specific plant process. One such sound could be the buzzing of bees. In a process referred to as buzz pollination, bumblebees stimulate a flower to release its pollen by rapidly vibrating their wing muscles without actually flapping their wings, leading to a high-frequency vibration. While this vibration can be heard (it’s the buzz we hear when a bee flies by), the pollen release necessitates a physical contact between the vibrating bee and the flower. So just as deaf people can feel and respond to vibrations in music, flowers feel and respond to bumblebee vibrations, without necessarily hearing them. But conceivably, the sound of the vibrations could also affect the flower in some yet undetected way.

In a similar vein, Roman Zweifel and Fabienne Zeugin from the University of Bern in Switzerland have reported ultrasonic vibrations emanating from pine and oak trees during a drought. These vibrations result from changes in the water content of the water-transporting xylem vessels. While these sounds are passive results of physical forces (in the same way that a rock crashing off a cliff makes a noise), perhaps these ultrasonic vibrations are used as a signal by other trees to prepare for dry conditions?

If scientists are going to properly study plant responses to sound waves, we need to understand that if a plant needs to hear, then its auditory system would be much different from what has evolved in animals. In addition to the few examples above, perhaps some plants sense minuscule sounds that might be created by tiny organisms. That kind of system may be off the radar screen of most physiological tools.

While these possibilities are interesting to ponder, in lieu of any hard data to the contrary we must conclude for now that plants are deaf and that they did not acquire this sense during evolution. The great evolutionary biologist Theodosius Dobzhansky wrote, “Nothing in biology makes sense except in the light of evolution.” Considering this, perhaps we can understand why hearing, as opposed to the other senses we’ve covered, isn’t really needed by plants.

The evolutionary advantage created from hearing in humans and other animals serves as one way our bodies warn us of potentially dangerous situations. Our early human ancestors could hear a dangerous predator stalking them through the forest. We notice the faint footsteps of someone following us late at night on a poorly lit street. We hear the motor of an approaching car. Hearing also enables rapid communication between individuals and between animals. Elephants can find each other across vast distances by vocalizing subsonic waves that rumble around objects and travel for miles. A dolphin pod can find a dolphin pup lost in the ocean through its distress chirps, and emperor penguins use distinct calls to find their mates. What’s common in all of these situations is that sound enables a rapid communication of information and a response, which is often movement—fleeing from a fire, escaping from attack, finding family.

As we’ve seen, plants are sessile organisms, secured to the ground by their roots. While they can grow toward the sun and bend with gravity, they can’t flee. They can’t escape. They don’t migrate with the seasons. They remain anchored in the face of an ever-changing environment. Plants also operate on a different timescale from animals. Their movements, with the conspicuous exception of plants like Mimosa and the Venus flytrap, are quite slow and are not easily noted by the human eye. As such, plants have no need for detailed communication that could allow for a quick retreat. The rapid audible signals we’re used to in our world are irrelevant to a plant. Plants lack the structures for purposeful vocalization, and the sounds of leaves in the wind or branches cracking under our feet do not communicate anything to the plant. For hundreds of millions of years plants have thrived on earth, and the nearly 400,000 species of plants have conquered every habitat without ever hearing a sound. But although they may be deaf, plants are acutely aware of where they are, what direction they’re growing, and how they move.