Abstract
In-air hearing in birds has been thoroughly investigated. Sound provides birds with auditory information for species and individual recognition from their complex vocalizations, as well as cues while foraging and for avoiding predators. Some 10% of existing species of birds obtain their food under the water surface. Whether some of these birds make use of acoustic cues while underwater is unknown. An interesting species in this respect is the great cormorant (Phalacrocorax carbo), being one of the most effective marine predators and relying on the aquatic environment for food year round. Here, its underwater hearing abilities were investigated using psychophysics, where the bird learned to detect the presence or absence of a tone while submerged. The greatest sensitivity was found at 2 kHz, with an underwater hearing threshold of 71 dB re 1 μPa rms. The great cormorant is better at hearing underwater than expected, and the hearing thresholds are comparable to seals and toothed whales in the frequency band 1–4 kHz. This opens up the possibility of cormorants and other aquatic birds having special adaptations for underwater hearing and making use of underwater acoustic cues from, e.g., conspecifics, their surroundings, as well as prey and predators.
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References
Catchpole C, Slater P (2008) Bird song: biological themes and variations. Cambridge University Press, Cambridge
Crowell SC (2014) In-air and underwater hearing in ducks. Doctoral dissertation, University of Maryland
Crowell SC (2016) Measuring in-air and underwater hearing in seabirds the effects of noise on aquatic life II. Springer, Berlin, pp 1155–1160
Dooling RJ (1992) Hearing in birds the evolutionary biology of hearing. Springer, Berlin, pp 545–559
Dooling RJ, Therrien SC (2012) Hearing in birds: what changes from air to water the effects of noise on aquatic life. Springer, Berlin, pp 77–82
Dooling RJ, Lohr B, Dent ML (2000a) Hearing in birds and reptiles comparative hearing: birds and reptiles. Springer, Berlin, pp 308–359
Dooling RJ, Lohr B, Dent ML (2000b) Hearing in Birds and reptiles. In: Dooling RJ, Fay RR, Popper AN (eds) Comparative hearing: birds and reptiles (Vol. 13). Springer-Verlag, New York
Dooling RJ, Leek MR, Gleich O, Dent ML (2002) Auditory temporal resolution in birds: discrimination of harmonic complexes. J Acoust Soc Am 112(2):748–759
Erbe C, Farmer DM (1998) Masked hearing thresholds of a beluga whale (Delphinapterus leucas) in icebreaker noise. Deep-Sea Res II Top Stud Oceanogr 45(7):1373–1388
Finney DJ (1971) Probit analysis, 3d edn. Cambridge University Press, Cambridge
Frantzis A (1998) Does acoustic testing strand whales? Nature 392(6671):29
Gellermann LW (1933) Chance orders of alternating stimuli in visual discrimination experiments. The Pedagogical Seminary and Journal of Genetic Psychology 42(1):206–208
Gescheider G (1997) Psychophysics: the fundamentals, 3rd edn. Lawrence Erlbaum Associates, Mahwah
Grémillet D (1997) Catch per unit effort, foraging efficiency, and parental investment in breeding great cormorants (Phalacrocorax carbo carbo). ICES Journal of Marine Science: Journal du Conseil 54(4):635–644
Grémillet D, Chauvin CC, Wilson RP, Le Maho Y & Wanless S (2005) Unusual feather structure allows partial plumage wettability in diving great cormorants Phalacrocorax carbo. J Avian Biol 36:57–63
Gremillet D, Kuntz G, Gilbert C, Woakes AJ, Butler PJ, le Maho Y (2005) Cormorants dive through the Polar night. Biol Lett 1(4):469–471. doi:10.1098/rsbl.2005.0356
Grémillet D, Nazirides T, Nikolaou H, Crivelli AJ (2012) Fish are not safe from great cormorants in turbid water. Aquat Biol 15(2):187–194
Johansen S, Larsen ON, Christensen-Dalsgaard J, Seidelin L, Huulvej T, Jensen K, Lunneryd S-G, Boström M, Wahlberg M (2016) In-air and underwater hearing in the great cormorant (Phalacrocorax carbo sinensis) the effects of noise on aquatic life II. Springer, Berlin, pp 505–512
Johnson CS (1967) Sound detection thresholds in marine mammals. Marine bio-acoustics 2:247–260
Kastak D, Schusterman RJ (1998) Low-frequency amphibious hearing in pinnipeds: methods, measurements, noise, and ecology. J Acoust Soc Am 103(4):2216–2228
Kastelein RA, Hoek L, de Jong CA, Wensveen PJ (2010) The effect of signal duration on the underwater detection thresholds of a harbor porpoise (Phocoena phocoena) for single frequency-modulated tonal signals between 0.25 and 160 kHz. J Acoust Soc Am 128(5):3211–3222
Kastelein RA, van den Belt I, Helder-Hoek L, Gransier R, Johansson T (2015) Behavioral responses of a harbor porpoise (Phocoena phocoena) to 25-kHz FM sonar signals. Aquat Mamm 41(3):311–326. doi:10.1578/am.41.3.2015.311
Kierl N, Johnston C (2010) Sound production in the pygmy sculpin Cottus paulus (Cottidae) during courtship and agonistic behaviours. J Fish Biol 77(6):1268–1281
Konishi M (1973) How the owl tracks its prey: experiments with trained barn owls reveal how their acute sense of hearing enables them to catch prey in the dark. Am Sci 61(4):414–424
Lewison R et al (2012) Research priorities for seabirds: improving conservation and management in the 21st century. Endanger Species Res 17(2):93–121
Marler PR & Slabbekoorn H (2004) Nature’s music: the science of birdsong. Academic Press, Boston
Maxwell A, Hansen KA, Ortiz ST, Larsen ON, Siebert U & Wahlberg M (2017) In-air hearing of the great cormorant (Phalacrocorax carbo). Biology Open, bio. 023879
Medwin H & Clay CS (1998) Fundamentals of Acoustical Oceanography. Academic Press, New York, p 24
Nachtigall PE, Au WW, Pawloski J (1996) Low-frequency hearing in three species of odontocetes. J Acoust Soc Am 100(4):2611–2611
Popper A, Hawkins A (2011) The effects of noise on aquatic life (Vol. 730). Springer Science & Business Media, Berlin
Popper AN, Hawkins A (2015) The effects of noise on aquatic life II (Vol. 875). Springer, Berlin
Proakis JG, Manolakis DG (1996) Digital signal processing, 4th edn. Pearson Prentice Hall, Upper Saddle River
Reichmuth C, Hold MM, Muslow J, Sills JM, Southall BL (2013) Comparative assessment of amphibious hearing in pinnipeds. J Comp Physiol A 199:491–507. doi:10.1007/s00359-013-0813-y)
Sills JM, Southall BL, Reichmuth C (2014) Amphibious hearing in spotted seals (Phoca largha): underwater audiograms, aerial audiograms and critical ratio measurements. J Exp Biol 217(5):726–734
Sills JM, Southall BL, Reichmuth C (2015) Amphibious hearing in ringed seals (Pusa hispida): underwater audiograms, aerial audiograms and critical ratio measurements. J Exp Biol 218(14):2250–2259
Strod T, Arad Z, Izhaki I, Katzir G (2004) Cormorants keep their power: visual resolution in a pursuit-diving bird under amphibious and turbid conditions. Curr Biol 14(10):R376–R377. doi:10.1016/j.cub.2004.05.009
Thewissen JG, Nummela S (2008) Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. Univ of California Press, Berkeley
Tougaard J, Carstensen J, Teilmann J, Skov H, Rasmussen P (2009) Pile driving zone of responsiveness extends beyond 20 km for harbor porpoises (Phocoena phocoena (L.)). J Acoust Soc Am 126(1):11–14
Wahlberg M, Westerberg H (2003) Sounds produced by herring (Clupea harengus) bubble release. Aquat Living Resour 16(3):271–275
Watanabe YY, Takahashi A, Sato K, Viviant M, Bost CA (2011) Poor flight performance in deep-diving cormorants. J Exp Biol 214(Pt 3):412–421. doi:10.1242/jeb.050161
White CR, Day N, Butler PJ, Martin GR (2007) Vision and foraging in cormorants: more like herons than hawks? PLoS One 2(7):e639. doi:10.1371/journal.pone.0000639
White C, Butler PJ, Grémillet D, Martin GR (2008) Behavioural strategies of cormorants (Phalacrocoracidae) foraging under challenging light conditions. Ibis 150(s1):231–239
Acknowledgements
We thank the many trainers and volunteers that have helped with the husbandry and training of the cormorants, especially L. Seidelin and S. Johansen. This work is funded by grants from the Danish Council for Independent Research | Natural Sciences, the Carlsberg Foundation, and a grant from the Swedish Environmental Protection Agency.
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Conceptualization, K. A. H., O. N. L., AND M. W.; Methodology, K. A. H. and M. W.; Software, M. W.; Investigation, K. A. H.; Formal analysis, K. A. H., A.M., AND M. W.; Funding acquisition, M. W., O. N. L., and U. S.; Writing-original draft, K. A. H. and M. W.; Review and editing, A. M., O. N. L., and U. S.
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Communicated by: Sven Thatje
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Hansen, K.A., Maxwell, A., Siebert, U. et al. Great cormorants (Phalacrocorax carbo) can detect auditory cues while diving. Sci Nat 104, 45 (2017). https://doi.org/10.1007/s00114-017-1467-3
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DOI: https://doi.org/10.1007/s00114-017-1467-3
Keywords
- Aquatic birds
- Psychophysics
- Sensory adaptation
- Threshold
- Underwater acoustics