PROCEEDINGS of the23rd International Congress on Acoustics
9 to 13 September 2019 in Aachen, Germany

The Cormorant Ear – Adapted to Underwater Hearing?
Ole Næsbye LARSEN1; Magnus WAHLBERG2; Jakob CHRISTENSEN-DALSGAARD3
1

University of Southern Denmark, Denmark2

University of Southern Denmark, Denmark

3

University of Southern Denmark, Denmark

ABSTRACTDiving birds may spend several minutes underwater during foraging dives. However, surprisingly little isknown about avian underwater hearing. We do not know their sensitivity or even if they respond tounderwater sound. To help filling this gap we measured the audiograms of cormorants (Phalacrocorax carbosinensis) and studied their ear anatomy. Wild-caught fledglings were anesthetized and their auditory
brainstem response (ABR) to clicks and tone bursts was measured, first in an anechoic box in air and then ina large water-filled tank with their head and neck submerged 10 cm below the surface. The overall shape of
their air-audiograms was like that reported for birds of the same size in air. The bandwidth and slopes of theiraudiograms were similar in air and water. However, in air the highest sensitivity was found at 2 kHz, whereas
it was displaced towards lower frequencies underwater. These results suggest that cormorants have rather
poor in-air hearing compared to similar-sized birds. Their underwater hearing sensitivity, however, is higher
than what would have been expected for purely air-adapted ears. A possible reason for the poor in-air
sensitivity is the special ear anatomy with the central eardrum shaped as a rigid piston like in turtles.
Keywords: Audiogram, Auditory threshold curves, Great cormorant

1. INTRODUCTION
In contrast to marine mammals little is known about the underwater hearing capabilities of diving
birds. Since some diving birds may reach the same depths as marine mammals and experience the samepotentially harmful anthropogenic underwater noise levels, it is important to obtain information about
their underwater hearing.
Cormorants feed exclusively on fish and are known for their impressive foraging efficiency (1).
During underwater pursuit of prey, they seem to rely mainly on vision, but their visual acuity is verylow (2). So, they may use supplementary sensory information, for instance auditory information on
prey movement and possible communication sounds. Therefore, they may be adapted to hearing
underwater. They may have adaptations that protect their ears during diving and they may haveadaptations that ensures high sensitivity to underwater sounds. The aim of the present study was tocompare cormorant hearing in air with that underwater by measuring their hearing threshold curves inthe two media.

2. MATERIAL AND METHODS
2.1 Experimental Subjects
Since it was not possible to use adult specimens, we collected fledglings from the nest in cormorantcolonies and used 12 specimens for this study.
2.2 ABR Recordings
To measure their hearing threshold curves we used a setup similar to that of Christensen -Dalsgaard
et al. (3) to record auditory evoked potential supposed to represent auditory brainstem responses
1

onl@biology.sdu.dk
magnus@biology.sdu.dk
3
jcd@biology.sdu.dk
2165

(ABR). Subdermal electrodes behind the ipsilateral ear opening (active electrode) and on top of thehead (inverting electrode) recorded the ABR-signals referred to ground by an electrode in the neck.
Stimulus sounds (clicks and 25 ms duration tone bursts) and recorded ABR-signals were created andprocessed by Tucker-Davis equipment as (3). In air the deeply anesthetized birds were placed in an
anechoic box with their ipsilateral ear 70 cm away from the speaker. In w ater their heads weresubmerged 10 cm below the water surface 45 cm from an underwater speaker, after subjecting the still
deeply anesthetized birds to tracheostomy, such that they kept voluntarily breathing during
measurements.
2.3 Ear AnatomyOuter and inner ear anatomy was investigated by dissecting and photographing the ear under asurgical microscope.

3. RESULTS
3.1 Threshold Curves
Threshold curves (sound pressure levels) of the 12 subjects generally had similar shapes but varied
greatly in sensitivity (ranges 15-30 dB in air and 10-40 dB underwater). Figure 1 shows a
representative example of threshold curves in air and underwater for a single specimen. In general, thelow-frequency slopes of the threshold curves were very similar, whereas the high -frequency slopes in
air were steeper than those underwater and the best frequency in air was at a higher frequency (2 kHz)
than underwater (1 kHz). However, the lowest threshold was much the same when comparing
ABR-responses in air and underwater.
Threshold curves may also be expressed in energy terms (sound intensity levels) by relating thedB-values to 1 pW/m 2 by further subtracting 36 dB from the underwater threshold curves in Figure 1(for further explanation of this conversion see e.g. 4).

Figure 1 – Threshold curves in air (triangles) and in water (circles) for a single fledgling (individual H). In air
the dB reference value is 20 µPa, whereas in water it is 1 µPa. To compare threshold curves in air and water
both have been referred to 20 µPa by subtracting 26 dB from the underwater threshold values (for further
explanation of conversion see e.g. 4)

166

3.2

AnatomyThe ear opening was comparatively small and easily compressible, and the ear canal was bent such thatthe eardrum was invisible from outside. The eardrum was difficult to delineate as it appeared very flat andthick with the extra-columella covering a substantial fraction of its inner surface.

4. DISCUSSION
4.1 Adaptations to Underwater Hearing
The cormorant threshold curves in air were shaped like those of other diving birds (5) but lesssensitive (6). In comparison, their underwater hearing thresholds were as good ( expressed as soundpressure levels) or better (expressed as sound intensity levels) than those in air. So, although we do notknow whether cormorants use their underwater hearing to obtain supplementary sensory information
during pursuit-dive foraging, they definitely have the potential of doing so.
The anatomy of the outer ear and ear canal could be interpreted to serve as protection of the ear
during diving. Their surprisingly high sensitivity under water could be caused by an anatomical
adaptation making the eardrum flat and thick, almost like that observed in turtles (3). A recent study(7) suggests that such a plate-like tympanum is more efficient than a protruding thin membrane incoupling sound energy in water to the inner ear.

5. CONCLUSIONS
The results suggest that cormorants have rather poor in-air hearing compared to similar-sized birds.
Their underwater hearing sensitivity, however, is higher than what would have been expected forpurely air-adapted ears. A possible reason for the poor in-air sensitivity is the special ear anatomy withthe central eardrum flat and thick, and shaped as a rigid piston like in turtles.

ACKNOWLEDGEMENTS
This study was funded by the Carlsberg Foundation (grants # 2009-01-0292, # 2012-01-0662, and# 2013-01-0917), and by the Danish Council for Independent Research | Natural Sciences (grant #DFF-4002-00536).

REFERENCES1. Grémillet D, Argentin G, Schulte B, Culik BM. Flexible foraging techniques in breeding Cormorants
Phalacrocorax carbo and Shags Phalacrocorax aristotelis: benthic or pelagic feeding? Ibis 1998;140:
113–119.
2. White CR, Day N, Butler PJ, Martin GR. Vision and foraging in cormorants. More like herons thanhawks? PLoS ONE 2007;2(7):e609.
3. Christensen-Dalsgaard J, Brandt C, Willis KL, Christensen CB, Ketten D, Edds-Walton P, Fay RR,Madsen PT, Carr EC. Specialization for underwater hearing by the tympanic middle ear of the turtle,Trachemys scripta elegans. Proc. Roy. Soc. B, 2012;279:2816-2824.
4. Larsen ON, Wahlberg M. Sound and Sound Sources. In: Brown CH, Riede T, editors. Comparative
Bioacoustics: An Overview, Sharjah, UME: Bentham Science Publishers; 2017. p. 3-62.
5. Crowell SC, Wells-Berlin AM, Carr CE, Olsen GH, Therrien RE, Yannuzzi SE, Ketten DR. A
comparison of auditory brainstem responses across diving bird species. J. Comp. Physiol. A 2015;
201(8):803-815.
6. Maxwell A, Hansen KA, Ortiz ST, Larsen ON, Siebert U, Wahlberg M. In-air hearing of the great
cormorant (Phalacrocorax carbo). Biology Open 2017:6(4):496-502.
7. Vedurmudi AP, Christensen-Dalsgaard J, van Hemmen JL. Modeling underwater hearing and soundlocalization in the frog Xenopus laevis. J. Acoust. Soc. Am. 2018;144(5):3010-3021.

167