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The myth of the silent world: How centuries of anatomical skepticism veiled fish communication

11 min read

In Brief

  • Fish were historically presumed to be mute and deaf based on anthropocentric anatomical comparisons (lacking lungs and external ears) and the mistaken belief that water was a poor sound conductor.
  • Anecdotal evidence from mariners and systematic early scientific inquiry, such as M. Dufossé's work, consistently challenged this view by documenting complex, intentional sounds often linked to breeding and courtship.
  • The mystery of fish hearing was resolved by recognizing the functionality of the inner ear, which perceives vibrations transmitted through the skull and often the swim-bladder, compensating for the lack of an external ear.
  • The 'silent world' concept was definitively overturned by the understanding that water is an extremely efficient conductor of sound, making vocalization a crucial adaptive trait for survival, defense, and navigation in aquatic environments.

For much of natural history, the world beneath the water's surface was considered a realm of profound silence [1]. Fish, in particular, were often presented as the archetype of muteness, a stark contrast to the vocally expressive birds and terrestrial animals [2, 3]. This perception was deeply rooted in anatomical assumptions; lacking the familiar lungs, windpipes, and external ears of land-dwelling vertebrates, fish seemed ill-equipped for both producing and perceiving sound [4, 5, 6]. The very medium they inhabited, water, was frequently misunderstood as an environment hostile to acoustics, further cementing the image of a silent, unhearing aquatic existence [7].

This established view, however, was persistently troubled by a current of contradictory evidence. For centuries, mariners and coastal inhabitants reported hearing inexplicable and often elaborate sounds emanating from the depths—strange harmonies described as a mixture of organ music, ringing bells, and guttural cries [8, 9]. Simultaneously, empirical observations demonstrated that fish were not oblivious to acoustic stimuli. From Pliny the Elder's accounts of fish in imperial ponds responding to their names to more common observations of them being summoned by a clapping of hands, it was clear that they could, in some manner, perceive sound [10, 11, 12]. This created a fundamental tension between the anatomical theories that declared fish deaf and mute, and the lived experiences that suggested otherwise.

The journey to reconcile these conflicting perspectives constitutes a significant chapter in the history of zoology. It required moving beyond anthropocentric comparisons and delving into the unique physics of underwater sound and the specialized biology of aquatic creatures. This exploration traces the long-standing debate, examining the foundations of scientific skepticism, the gradual accumulation of evidence for fish vocalization, and the evolving understanding of how aquatic animals perceive their world through vibration and sound, ultimately revealing that the supposed 'world of silence' is, in fact, a vibrant and complex soundscape [13].

The presumption of silence: Anatomical skepticism and the mute fish

The classical and early modern conviction that fish were silent was primarily an argument from anatomy. Ancient authorities like Aristotle established a foundational view by observing that fish lack the physiological structures associated with voice in terrestrial animals, namely lungs and a pharynx [14]. Any noises they produced were therefore dismissed as unintentional, mechanical byproducts, such as squeaks from their gills, rather than true vocalizations . This perspective proved remarkably durable, shaping scientific thought for centuries and leading to the widely held axiom that fish were necessarily mute . The apparent absence of an external ear further bolstered the case, leading to the logical, if incorrect, conclusion that fish were also deaf [15, 16].

This biological skepticism was reinforced by prevailing beliefs about physics. Water was often incorrectly characterized as a poor conductor, or even a non-conductor, of sound, providing a seemingly scientific basis for the presumed deafness of aquatic life . It was argued that generating a sound underwater would demand a considerable amount of power, likely beyond the capabilities of most marine creatures [17]. This led some naturalists to conclude that even if fish could make noises, they would remain inaudible and irrelevant to human observers [18]. From an evolutionary standpoint, the first true voice was thought to have emerged much later with amphibians, leaving the entire class of fishes in a primordial, silent state [19].

Cultural perceptions mirrored and magnified these scientific assumptions. The common expression 'cold as a fish' reflected a broader view of these creatures as possessing minimal sensibility and existing in a state far removed from the emotional and social complexities associated with vocal communication [20]. Human experience underwater seemed to confirm this; divers reported a muffled, quiet environment where even powerful sounds like a cannon shot were dulled, reinforcing the conception of the sea as a 'world of silence' [21]. This confluence of anatomical reasoning, flawed physics, and cultural bias created a powerful and long-lasting paradigm of the silent fish.

Challenging the silence: Anecdotal evidence and early investigations

Despite the prevailing scientific consensus, a rich collection of anecdotal evidence consistently challenged the notion of a silent sea. Experienced observers, particularly sailors and fishermen, recounted encounters with mysterious and complex underwater sounds . These were not simple noises but often described as elaborate acoustic phenomena, including musical tones and bell-like harmonies that seemed to originate from directly beneath their vessels . In parallel, long-standing practices suggested that fish were responsive to sound. Pliny's observation that fish in captivity could be trained to respond to specific calls or the sound of clapping hands was a well-known example that demonstrated a clear auditory capacity . Such accounts, while often dismissed, formed a body of empirical counter-evidence that could not be entirely ignored.

The transition from folklore to formal inquiry was marked by the work of researchers like M. Dufossé, who undertook the first systematic studies of fish vocalizations. By coining the term 'Fish-noise,' Dufossé legitimized the phenomenon as a subject of scientific investigation [22]. He moved beyond simple acknowledgment of the sounds, categorizing them based on their acoustic properties—such as musical tones, blowing sounds, and creaking noises—and began to explore the diverse mechanisms by which they were produced [23]. This work was crucial in shifting the debate from whether fish made noise to how and why they did so.

A key insight that strengthened the case for intentional vocalization was the link between sound production and specific behaviors, especially reproduction. Naturalists observed that many fish noises were most frequent and intense during the spawning season, and were often produced exclusively by males [24]. This suggested that the sounds served a distinct biological function, likely related to courtship, territorial defense, or species recognition . One account even describes a male fish gritting its teeth as part of a courtship display to a female [25]. Tying sound to a clear evolutionary advantage provided a powerful argument against the view of fish noises as random, meaningless byproducts.

The anatomy of aquatic sound: Re-examining how fish hear and speak

A deeper investigation into fish anatomy revealed specialized mechanisms for sound production that had been previously overlooked. The swim-bladder, an internal gas-filled organ, was identified as a primary source of sound in many species, capable of producing noises when vibrated by surrounding muscles [26, 27, 28]. While its function at extreme depths was questioned due to immense pressure, its role in sound production in shallower waters became widely accepted . Other documented methods were equally varied, including the grinding of pharyngeal teeth during courtship displays and the use of other specialized sacs . This anatomical diversity helped explain the wide range of sounds—from the 'drumming' of the drum-fish to the squeaks of eels—that had been cataloged by observers [29].

The puzzle of fish hearing likewise depended on a re-evaluation of their anatomy. The initial dismissal based on the lack of an external ear gave way to the recognition that fish possess well-developed inner ears, structurally similar to those of higher vertebrates [30]. While some texts continued to flatly deny the existence of hearing organs , a more nuanced view emerged that acknowledged a simple but functional auditory system . Researchers proposed that sound vibrations were transmitted to this inner ear not through an ear canal, but via the bones of the skull and, in some species, through a direct connection to the swim-bladder, which acts as a resonator [31].

With the confirmation of auditory organs, the debate evolved to question what and how fish hear. One school of thought suggested that their senses were primarily attuned to low-frequency vibrations and changes in water pressure, perceived through both the inner ear and the lateral line system, rather than to 'sound' as humans experience it [33]. However, other evidence pointed to a more acute sense of hearing. The fact that fish could be startled by loud noises, killed by the shockwave of underwater explosions, or alerted by the tapping on the side of a boat all suggested a high sensitivity to acoustic vibrations [34, 35]. This led to the compelling argument that their auditory apparatus, though different, was exquisitely adapted to their environment [32].

From a silent world to a sonic sea

A critical turning point in the debate was the corrected understanding of underwater physics. The long-held belief that water was an acoustic dead zone was overturned by the scientific recognition that it is, in fact, a far more efficient conductor of sound than air [36, 37]. This realization meant that vocalizations could travel significant distances underwater, making sound a highly effective medium for communication . This physical principle aligned perfectly with fishermen's practical knowledge that sharp vibrations transmitted through the water, like knocking on a boat's hull, were far more likely to disturb fish than loud conversations carried through the air [38].

The discussion was also profoundly shaped by an increasing awareness of the limits of human perception. The fact that human divers experience the underwater world as largely silent was recognized as a subjective limitation, not an objective reality . Naturalists began to speculate that, much like certain insects, some fish might produce sounds at frequencies beyond the range of human hearing [39, 40]. The argument was simple: the existence of auditory organs in species that appeared to be 'dumb' did not prove they were useless; it might only prove that human ears were incapable of detecting their signals .

Ultimately, the evidence converged on a functional and evolutionary understanding of the aquatic soundscape. The presence of auditory organs, even in seemingly voiceless species, strongly implied a crucial survival advantage . Hearing provides fish with vital information about their environment, allowing them to detect the movements of predators and prey and to react to disturbances that signal danger . The pairing of vocal organs with specific life events, such as breeding, and their particular utility in habitats with low visibility, cemented the view that sound production is a key adaptive trait in many species .

✻

The lengthy scientific journey from dismissing fish as mute and deaf to recognizing their complex sonic lives illustrates a fundamental shift in biological inquiry. It marks a transition from reasoning based on superficial, human-centric anatomical comparisons to a more nuanced understanding grounded in behavioral ecology, physiology, and physics . The concept of the 'silent world' was ultimately revealed to be a projection of human sensory limitations onto a foreign environment, a failure to appreciate that life adapts to its surroundings in ways not immediately obvious to a terrestrial observer .

The acknowledgment of an underwater soundscape does more than simply correct an old scientific misconception; it fundamentally reshapes our perception of fish and their world. Far from being the cold, unfeeling creatures of aphorism, they are participants in a vibrant acoustic realm, using and perceiving sound for survival, courtship, and navigation . The discovery of their voices and auditory senses reveals a layer of complexity previously unimagined, transforming the silent depths into a space filled with communication that humanity was simply not equipped to hear for centuries .