Friday 2 August 2024
Fish hearing vs. Darwin.
Study Unravels the Mystery of Fish Hearing
A newly published study in the journal Nature concerning fish hearing has apparently unraveled the mechanism for how they determine the direction of sound.1 For a long time it was believed that fish did not possess any sense of hearing. One reason was because they do not have external ears. That ignored the fact that hearing is accomplished by the inner ear in most animals. It was Nobel Prize-winner Karl von Frisch who conducted experiments in the 1930s that proved fish can hear sounds. Since then, it has been known that fish can determine the direction of sounds. Yet an explanation of how this is accomplished has been elusive.
Human Hearing
It is instructive first to understand how humans and other vertebrate animals determine the direction of sound. Humans use the time difference between the arrival of sound waves at the two ears. This is called the interaural time difference (ITD). Humans can discern the horizontal direction to within 2 degrees, which translates to a time difference of 11 microseconds.2 That means human brains have an extremely well-designed neural network to achieve that level of performance. One theory is that there is a network of neurons that “use axons as delay lines and to measure small time differences precisely.”3 In addition, vertebrates detect the differences in sound wave pressure between the ears, which is also an aid in determining direction.
Challenge of Sound Detection Underwater
Detecting and processing sound underwater presents more problems than in the air. One is that the speed of sound is approximately five times faster in water than in air. That means that the ITD is significantly shorter, which makes it more challenging to measure the difference in the arrival time between two receptors in an animal. The detected pressure differences are also smaller underwater. In addition, sound pressure in water has no directional component. Due to these and other technical problems the prevailing models indicated that it should not be possible for fish to determine the direction of a source of sound.
Evidence of Fish Detection of Sound Direction
There is a large body of experimental evidence showing that fish can determine the direction of sound. Directional hearing is essential to a number of fish behaviors, including finding prey, avoiding predators, and locating mates. The ability to move in the direction of the source of sound is called phonotaxis. One example in fish is that the females of some species will seek the mating call of males. That includes the ability to distinguish different species, as fish bioacoustics scientists Anthony Hawkins and Arthur Popper explain, “Behavioral studies of sound communication have indicated that fish discriminate between calls on the basis of differences in repetition rate and duration, rather than frequency or bandwidth.”4 It should not be surprising that fish have very good hearing capabilities because as Jonathan Balcombe, author of What a Fish Knows, writes, “Despite the common assumption that fishes are silent, they actually have more ways of producing sounds than any other group of vertebrate animals…Fishes produce a veritable symphony of sounds…So notable are the sounds of some fishes that we have named the fishes accordingly: grunts, drums, trumpeters, croakers, sea robins, and grunters.”5
Experiments were conducted in which Atlantic cod and haddock were conditioned to respond to a pulsed tone from loudspeakers at different horizontal angles. The results showed that the fish readily detected the difference when the loudspeakers were separated by 20 degrees or more.6 Hawkins and Popper also state that the experiments “demonstrated that the cod is well able to discriminate between separate sound sources in 3D space.”7 There is evidence in mammals for a correlation between the field of vision and the ability to determine the direction of sound.8 In other words, the narrower the field of vision the more accurate the sound localization that appears to be required. In the case of fish, since they typically have a very wide field of vision, their localization of sound probably does not need to be that accurate. Hence, as was found in the described experiment, localization within about 20 degrees is likely sufficient. The fact that fish have the ability to determine the direction of sound and employ it in numerous behaviors made it all the more confounding why scientists had been unable to determine the mechanism.
One important characteristic of fish that does help sound detection is that they are acoustically transparent. This characteristic is useful because, in addition to pressure, the transmission of sound in any medium occurs through the oscillation of pressure and motion. In addition to the oscillatory change of the pressure wave, underwater sound also consists of a to-and-fro motion of particles in the direction of transmission. This phenomenon is called particle motion which “can be measured in terms of displacement, velocity, or acceleration, (and) differs from the sound pressure in that it is inherently directional, and all the motion parameters are vector quantities.”9 It turns out that this phenomenon of sound transmission in water is crucial as, “This mechanism for the direct detection of particle motion by the otolith organs is found in all fishes.”10Detection of this motion isn’t trivial since, “The to-and-fro displacements of the very small body of water are of the order of nanometers.”11 At first it might seem simple to determine direction based on particle motion since the motion is directly in line with the propagation of the sound wave. The problem, however, is that because the motion is back-and-forth, there is an ambiguity of 180 degrees in the direction.
The Experiment
For the experiment documented in the Nature paper the researchers tested hearing capability in Danionella cerebrum, one of the smallest teleost (bony) fish. An additional problem for hearing in small fish is that the distance between the inner ears is relatively short. In the case of D. cerebrum it is only about 0.6 millimeters, which is several orders of magnitude smaller than the wavelength of sound (approximately 150 millimeters). That makes it difficult to measure the phase of the detected pressure wave. The experiment was able to simulate and control a number of variables associated with sound (notably pressure and motion) and observed how the fish reacted. In addition, during the experiment a laser scanning microscope was used to examine the fish hearing auditory structures. This enabled the researchers to compare the reaction of the auditory structures with the various models.
Directional Hearing Mechanism
The study evaluated several different theories and models of potential mechanisms for determining direction. After the researchers compared the experimental results with the models, the evidence provided the most validation for one model, originally proposed by zoologist Arie Schuijf in 1975. The Schuijf model is based on the comparison of pressure and particle motion. Fish are able to detect the motion of pressure and particle motion separately, using individual detectors. The detection of pressure occurs in the swim bladder as, “All known sound pressure sensors in fish are based on compressible gas-filled organs.”12 The swim bladder is the organ used by bony fish to control their buoyancy. Particle motion can be detected because, being acoustically transparent, tissue in the fish is coupled to the motion of the water as it moves through the fish. The two measurements can then be compared and used to estimate the incoming direction of sound. The reason this is possible is because the pressure and particle motion are out of phase. When pressure is highest the particle motion is away from the source. When pressure is lowest the particle motion is toward the source.
As described by the authors of the paper, this physical characteristic of underwater acoustics provides the basis for the directional hearing algorithm. There is a neural mechanism that uses these two sensory inputs to estimate the direction that the sound is coming from. In addition to highly sensitive sensors it must also include an accurate internal clock to determine when the two inputs are to be compared. The fish directional hearing algorithm appears to be another example of a complex programmed behavior in animals.13 However, as indicated in a related Nature article, “We do not yet know what happens in the brain and how it interprets information from the inner ear about the phase and amplitude of sounds.”14
Some experiments also appear to indicate that fishes can estimate distance based on the information provided by pressure and particle motion sensors. The ability to estimate the distance of the source of sound is a hearing capability not possessed by humans. Some species of fish can detect ultrasound up to frequencies of 180,000 Hertz.15 Human hearing capability is typically up to 20,000 Hertz. Very impressive capabilities for animals that scientists once thought had no hearing ability at all!
Notes
Veith, et al., “The mechanism for directional hearing in fish,” Nature, Vol. 631, 4 July 2024, 118-23.
Mark F. Bear, Barry W. Connors, Michael A. Paradiso, Neuroscience (Philadelphia: Lippincott Williams & Wilkins, 2007), 369.
Bear, et al., Neuroscience, 370.
Anthony D. Hawkins, Arthur N. Popper, “Directional hearing and sound source localization by fishes,” J. Acoust. Soc. Am. 144, 3329-3350, December 14, 2018.
Jonathan Balcombe. What a Fish Knows (New York: Scientific American, 2016), 40-41.
Hawkins and Popper, “Directional hearing and sound source localization by fishes.”
Hawkins and Popper, “Directional hearing and sound source localization by fishes.”
Henry E. Heffner, Rickye S. Heffner, “The evolution of mammalian hearing,” AIP Conf. Proc. 1965, 130001, May 31, 2018.
Popper, et al., “Examining the Hearing Abilities of Fishes,” J. Acoust. Soc. Am., 146, 948–955 (2019).
Popper and Hawkins, “The importance of particle motion to fishes and invertebrates.”
Arthur N. Popper, Anthony D. Hawkins, “The importance of particle motion to fishes and invertebrates,” J. Acoust. Soc. Am. 143, 470-488, January 29, 2018.
Veith, et al., “The mechanism for directional hearing in fish,” 123.
Eric Cassell, Animal Algorithms (Seattle: Discovery Institute Press, 2021).
Catherine E. Carr, “How fish sense the direction of sound,” Nature, Vol. 631, 4 July 2024, 29.
Friedrich Ladich and Tanja Schulz-Mirbach, “Diversity in Fish Auditory Systems: One of the Riddles of Sensory Biology,” Front. Ecol. Evol. 4:28, 31 March 2016.
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