Infrasonic hearing in birds review

I’ve recently led a review paper on the subject of infrasonic hearing in birds, which is now published in Biological Reviews. The paper surveys the studies that have assessed infrasonic hearing in birds and presents various potential underlying anatomical and physiological traits that could be involved. In this post, I’ll summarize what I think are some of the interesting highlights from the review.

In terrestrial animals, hearing tests that go down to frequencies below 20 Hz (infrasound) are actually not all that common. However, the studies that we have available to date have demonstrated that a handful of mammals and birds can hear infrasound. Among bird species, infrasound sensitivity varies quite a bit. The rock dove and some birds in the order Galliformes (chicken, guinea fowl, and likely peafowl) are quite sensitive, while other birds such as budgerigar and mallard duck are quite insensitive. The infrasound sensitivity in the former group is in a similar range as those of mammals with excellent low frequency hearing abilities (elephants and black-tailed prairie dog).

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Rock dove, a bird known to detect infrasound (CC0 public domain image).

In nature, many of the sources of infrasound come from geophysical sources (e.g., colliding ocean waves, surf, earthquakes). One technical challenge that arises when interpreting the responses of freely behaving birds to natural infrasound sources is distinguishing a bird’s responses to infrasound from its responses to other concurrent non-acoustic fluctuations in atmospheric pressure. The non-acoustic pressure fluctuations (e.g., wind) can occur in the same frequency bands as infrasound, be of even greater magnitude than the infrasound, and can stimulate the ear. Laboratory tests are therefore an essential key to verify what birds can detect at infrasonic frequencies. We reviewed the different audiometry methods that have been used. Some of the more common methods have involved playback with subwoofers and training birds to recognize a sound, or presenting the sound through air volumes sealed over the eardrum and measuring neural responses.

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Budgerigar, a bird with poor sensitivity to infrasound (CC0 public domain image).

Which auditory mechanisms would promote the hearing of airborne infrasound? In general, the tympanic middle ear [i.e an eardrum and ear ossicle(s)] is quite important for detecting airborne sounds. Without the tympanic middle ear, hearing sensitivity to airborne sound is reduced significantly because a large portion of the sound reflects off the body surface. Therefore, having a middle ear that is very responsive at low frequencies is one major way that some birds could improve low-frequency hearing sensitivity. From theoretical work and studies in mammals, we know that this could be achieved by lowering the stiffness of the middle ear. This could be done by having larger cranial air cavities behind the eardrum and flexible ligaments attached to the ear ossicles. Large eardrums, which could resonate at lower frequencies, would also be beneficial (consider, for example, the ostrich, which has high middle ear vibrations at low frequencies).

In most birds, however, the middle ear vibrates maximally at relatively high frequencies, often at 2-5 kHz. As the frequency is lowered below this peak, middle ear vibration typically decreases approximately at a rate of 6 dB/octave (i.e., reduces by half every time the frequency is halved). At very low frequencies, the middle ear vibrations may decline to such low levels that alternative sound pathways to the ear should also be considered. We know that in animals lacking tympanic middle ears such as salamanders, snakes, and anurans, such ‘extratympanic’ pathways can dominate the auditory response at low frequencies. To demonstrate this possibility, we compared bird middle ear vibrations with vibrations from extratympanic body tissues, and presented a model for the vibrations for a solid sphere in a free field.

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Some of the bird ear structures considered in the context of infrasound perception (Figure 2 from the review).

The review next discusses mechanisms at the level of the inner ear and auditory receptors. We discuss how openings in the inner ear, such as the cochlear aqueduct and helicotrema, could affect how low frequencies are shunted within the inner ear. Neural recordings have indicated that the basilar papilla, the auditory end organ in birds, is responsive to infrasound in some species. It’s also plausible that vestibular organs could detect airborne infrasound, but this possibility has yet to be examined. For species that do respond well to infrasound, there are likely some specializations in the ‘electrical tuning’ of hair cells, in terms of the kinetics of the ion movement across the cell membranes, to allow the hair cell membrane potential to oscillate at very long periods.

Infrasonic hearing could be more widespread in birds and other terrestrial animals than is currently appreciated. This review should be a useful resource for future studies in this area. Check out the paper for all the details.

ZEYL, J.N., OUDEN, O. DEN, KÖPPL, C., ASSINK, J., CHRISTENSEN‐DALSGAARD, J., PATRICK, S.C. & CLUSELLA‐TRULLAS, S. (2020) Infrasonic hearing in birds: a review of audiometry and hypothesized structure–function relationships. Biological Reviews (Early view article). https://doi.org/10.1111/brv.12596

Fall Research Travels

It seems to be a good time to post a research update coming from the auditory physiology side of the project. I’m currently wrapping up a research trip to Europe, where I worked on multiple different components of the project with the other team members in the UK and Netherlands. Olivier and I also had a productive visit to a bird hearing expert earlier this week in Oldenburg, Germany.

I have been reviewing the scientific literature on low frequency hearing in birds, including the various experimental studies and hypothesized detection mechanisms. There are indeed many factors that can control the detection of low frequencies by birds. Sound vibrations move through the middle ear, inner ear, and auditory hair cells, ultimately becoming encoded into a neural signal at the end of the transmission line. At each of these levels, there are distinct structure-function relationships that will affect signal transmission. There is likely no single anatomical marker that will precisely reflect infrasonic hearing abilities, but the relevant anatomical parameters and how they might be expected to affect low frequency transmission is becoming clearer.

Multiple building blocks need to come together to pursue the big question, “do seabirds detect infrasound?”. One of these building blocks is a quantification of the large-scale patterns of auditory anatomy in seabirds. For this goal, I have been collecting microCT scans of seabird heads and skulls. In general, not a lot has been described on the auditory anatomy of seabirds.

The microCT images are quite cool to view and analyse. Below are microCT images of white-chinned petrel, Procellaria aequinoctialis (A). This species is commonly caught as bycatch from long-line fisheries vessels operating in South African waters, and that was my source for this particular specimen (thanks to folks at Capfish and BirdLife). You can even see a fish still in the throat and a bit of the hook apparatus on the lower right. Here are some additional images showing the reconstruction process for this technique. You can see clearly on this image the columella (middle ear bone of birds) and inner ear (B). After some analysis, the 3D models of specific components can be reconstructed (C,D).

One possible further application of the comparative microCT data is to use the 3D surface models to simulate acoustic transmission properties of the ear. This can be an option for animals for which direct hearing assessments are difficult, such as whales. The simulation models are then verified by direct vibrometric observation of middle ear. This technique might be a useful method for testing between the performance of different routes of acoustic stimulation. For example, the vibration transmission performance of the middle ear in tetrapod animals (including birds) generally declines towards low frequencies. Alternatively, sound at these very low frequencies might effectively couple to the whole body of the bird itself.

After some delay with getting permits  to collect seabird heads (partly due to restrictions related to the bird flu striking earlier in the year), we have the permissions we need and I hope to be examining many more species soon.4 in 1