Great cormorants (Phalacrocorax carbo) can detect auditory cues while diving

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.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Catchpole C, Slater P (2008) Bird song: biological themes and variations. Cambridge University Press, Cambridge

    Google Scholar 

  2. Crowell SC (2014) In-air and underwater hearing in ducks. Doctoral dissertation, University of Maryland

  3. Crowell SC (2016) Measuring in-air and underwater hearing in seabirds the effects of noise on aquatic life II. Springer, Berlin, pp 1155–1160

    Google Scholar 

  4. Dooling RJ (1992) Hearing in birds the evolutionary biology of hearing. Springer, Berlin, pp 545–559

    Google Scholar 

  5. 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

    Google Scholar 

  6. Dooling RJ, Lohr B, Dent ML (2000a) Hearing in birds and reptiles comparative hearing: birds and reptiles. Springer, Berlin, pp 308–359

    Google Scholar 

  7. 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

    Google Scholar 

  8. 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

    Article  PubMed  Google Scholar 

  9. 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

    Article  Google Scholar 

  10. Finney DJ (1971) Probit analysis, 3d edn. Cambridge University Press, Cambridge

    Google Scholar 

  11. Frantzis A (1998) Does acoustic testing strand whales? Nature 392(6671):29

    CAS  Article  PubMed  Google Scholar 

  12. Gellermann LW (1933) Chance orders of alternating stimuli in visual discrimination experiments. The Pedagogical Seminary and Journal of Genetic Psychology 42(1):206–208

    Article  Google Scholar 

  13. Gescheider G (1997) Psychophysics: the fundamentals, 3rd edn. Lawrence Erlbaum Associates, Mahwah

    Google Scholar 

  14. 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

    Article  Google Scholar 

  15. 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

  16. 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

    Article  PubMed  PubMed Central  Google Scholar 

  17. 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

    Article  Google Scholar 

  18. 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

  19. Johnson CS (1967) Sound detection thresholds in marine mammals. Marine bio-acoustics 2:247–260

    Google Scholar 

  20. Kastak D, Schusterman RJ (1998) Low-frequency amphibious hearing in pinnipeds: methods, measurements, noise, and ecology. J Acoust Soc Am 103(4):2216–2228

    CAS  Article  PubMed  Google Scholar 

  21. 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

    Article  PubMed  Google Scholar 

  22. 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

    Article  Google Scholar 

  23. 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

    CAS  Article  PubMed  Google Scholar 

  24. 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

    Google Scholar 

  25. Lewison R et al (2012) Research priorities for seabirds: improving conservation and management in the 21st century. Endanger Species Res 17(2):93–121

    Article  Google Scholar 

  26. Marler PR & Slabbekoorn H (2004) Nature’s music: the science of birdsong. Academic Press, Boston

  27. 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

  28. Medwin H & Clay CS (1998) Fundamentals of Acoustical Oceanography. Academic Press, New York, p 24

  29. Nachtigall PE, Au WW, Pawloski J (1996) Low-frequency hearing in three species of odontocetes. J Acoust Soc Am 100(4):2611–2611

    Article  Google Scholar 

  30. Popper A, Hawkins A (2011) The effects of noise on aquatic life (Vol. 730). Springer Science & Business Media, Berlin

    Google Scholar 

  31. Popper AN, Hawkins A (2015) The effects of noise on aquatic life II (Vol. 875). Springer, Berlin

    Google Scholar 

  32. Proakis JG, Manolakis DG (1996) Digital signal processing, 4th edn. Pearson Prentice Hall, Upper Saddle River

    Google Scholar 

  33. 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)

    Article  Google Scholar 

  34. 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

    Article  PubMed  Google Scholar 

  35. 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

    Article  PubMed  Google Scholar 

  36. 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

    CAS  Article  PubMed  Google Scholar 

  37. Thewissen JG, Nummela S (2008) Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. Univ of California Press, Berkeley

    Google Scholar 

  38. 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

    Article  PubMed  Google Scholar 

  39. Wahlberg M, Westerberg H (2003) Sounds produced by herring (Clupea harengus) bubble release. Aquat Living Resour 16(3):271–275

    Article  Google Scholar 

  40. 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

    Article  PubMed  Google Scholar 

  41. 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

    Article  PubMed  PubMed Central  Google Scholar 

  42. White C, Butler PJ, Grémillet D, Martin GR (2008) Behavioural strategies of cormorants (Phalacrocoracidae) foraging under challenging light conditions. Ibis 150(s1):231–239

Download references

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.

Author information

Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Kirstin Anderson Hansen.

Additional information

Communicated by: Sven Thatje

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Keywords

  • Aquatic birds
  • Psychophysics
  • Sensory adaptation
  • Threshold
  • Underwater acoustics