Abstract
There is little biological data available for diving birds because many live in hard-to-study, remote habitats. Only one species of diving bird, the black-footed penguin (Spheniscus demersus), has been studied in respect to auditory capabilities (Wever et al., Proc Natl Acad Sci USA 63:676–680, 1969). We, therefore, measured in-air auditory threshold in ten species of diving birds, using the auditory brainstem response (ABR). The average audiogram obtained for each species followed the U-shape typical of birds and many other animals. All species tested shared a common region of the greatest sensitivity, from 1000 to 3000 Hz, although audiograms differed significantly across species. Thresholds of all duck species tested were more similar to each other than to the two non-duck species tested. The red-throated loon (Gavia stellata) and northern gannet (Morus bassanus) exhibited the highest thresholds while the lowest thresholds belonged to the duck species, specifically the lesser scaup (Aythya affinis) and ruddy duck (Oxyura jamaicensis). Vocalization parameters were also measured for each species, and showed that with the exception of the common eider (Somateria mollisima), the peak frequency, i.e., frequency at the greatest intensity, of all species’ vocalizations measured here fell between 1000 and 3000 Hz, matching the bandwidth of the most sensitive hearing range.
Similar content being viewed by others
References
Amoser S, Ladich F (2005) Are hearing sensitivities of freshwater fish adapted to the ambient noise in their habitats? J Exp Biol 208:3533–3542
Aubin T, Jouventin P, Hildebrand C (2000) Penguins use the two-voice system to recognize each other. Proc Roy Soc B 267:1081–1087
Austin JE, Custer CM, Afton AD (1998) Lesser scaup (Aythya affinis). Birds of North America Online. http://bna.birds.cornell.edu.proxyum.researchport.umd.edu/bna/species/338. doi:10.2173/bna.338. Accessed 10 Mar 2014
Barr JF, Eberl C, Mcintyre JW (2000) Red-throated loon (Gavia stellata). Birds of North America Online. http://bna.birds.cornell.edu.proxy-um.researchport.umd.edu/bna/species/513. Accessed 10 Mar 2014
Beecher MD (1981) Development of parent-offspring recognition in birds. In: Aslin RK, Alberts JR, Petersen MR (eds) Development of perception, vol 1. Academic Press, New York, pp 45–66
Beuth JM (2013) Body composition, movement phenology and habitat use of common eider along the southern New England coast. Open Access Master’s Theses
Blickley JL, Blackwood D, Patricelli GL (2012) Experimental evidence for the effects of chronic anthropogenic noise on abundance of greater sage-grouse at leks. Conserv Biol 26:461–471
Bom N (1969) Effect of rain on underwater noise level. J Acoust Soc Am 45:150–156
Bordage D, Savard JPL (2011) Black scoter (Melanitta americana). Birds of North America Online. http://bna.birds.cornell.edu.proxy-um.researchport.umd.edu/bna/species/177. Accessed 10 Mar 2014
Borg E (1982) Auditory thresholds in rats of different age and strain. A behavioral and electrophysiological study. Hear Res 8(2):101–115
Borg W, Engström B (1983) Hearing thresholds in the rabbit: a behavioral and electrophysiological study. Acta Otolaryngol 95:19–26
Brittan-Powell EF, Dooling RJ (2004) Development of auditory sensitivity in budgerigars (Melopsittacus undulatus). J Acoust Soc Am 115:3092–3102
Brittan-Powell EF, Dooling RJ, Gleich O (2002) Auditory brainstem responses in adult budgerigars (Melopsittacus undulatus). J Acoust Soc Am 112(3):999–1008
Brittan-Powell EF, Lohr B, Hahn DC, Dooling RJ (2005) Auditory brainstem responses in the Eastern Screech Owl: an estimate of auditory thresholds. J Acoust Soc Am 188(1):314–321
Brittan-Powell EF, Dooling RJ, Ryals BM, Gleich O (2010) Electrophysiological and morphological development of the inner ear in Belgian waterslager canaries. J Acoust Soc Am 118:314–321
Brown PW, Fredrickson LH (1997) White-winged Scoter (Melanitta fusca). Birds of North America Online: http://bna.birds.cornell.edu.proxy-um.researchport.umd.edu/bna/species/274. Accessed 10 Mar 2014
Brua RB (2002) Ruddy duck (Oxyura jamaicensis). Birds of North America Online. http://bna.birds.cornell.edu.proxy-um.researchport.umd.edu/bna/species/696. Accessed 10 Mar 2014
Bureau of Ocean Energy and Management (2013) Determining offshore use by diving marine birds using satellite telemetry. Environmental studies program. http://www.boem.gov/uploadedFiles/BOEM/Environmental_Stewardship/Environmental_Studies/Renewable_Energy/AT%2012-02%20Diving%20Birds.pdf. Accessed 12 Feb 2014
Burkard R, Voigt HF (1989) Stimulus dependencies of the gerbil brainstem auditory evoked response (BAER): I. Effects of click level, rate and polarity. J Acoust Soc Am 85:2514–2525
Campo JL, Gil MG, Davila SG (2005) Effects of specific noise and music stimuli on stress and fear levels of laying hens of several breeds. Appl Anim Behav Sci 91:75–84
Caras ML, Brenowitz E, Rubel EW (2010) Peripheral auditory processing changes seasonally in Gambel’s white-crowned sparrow. J Comp Physiol A 196(8):581–599
Carney KM, Sydeman WJ (1999) A review of the human disturbance effects on nesting colonial waterbirds. Waterbirds: int J Waterbird. Biol 22(1):68–79
Carpenter JW (2013) Exotic animal formulary. Elsevier, St. Louis, MO
Carr CE, Soares D, Smolders J, Simon JZ (2009) Detection of interaural time differences in the alligator. J Neurosci 29(25):7978–7990
Cederholm JM, Froud KE, Wong AC, Ko M, Ryan AF, Housely GD (2012) Differential actions of isoflurane and ketamine-based anaesthetics on cochlear function in the mouse. Hear Res 292(1–2):71–79
Chapdelaine G, Dupuis P, Reed A (1986) Distribution, abondance at fluctuation des populations d’eider a duvet dans l’estuaire et le golfe du Saint-Laurent. In: Reed A (ed) Eider ducks in Canada. Can Wild Serv Rep Ser no 47, Ottawa, pp 6–19
Deng X, Wanger HJ, Popper AN (2002) Messages from the bottom of the Atlantic Ocean: comparative studies of anatomy and ultrastructure of the inner ears of several gadiform deep-sea fishes. Abst Assn Res Otolaryngol 25:101
Dooling RJ (2002) Avian hearing and the avoidance of wind turbines. National Renewable Energy Laboratory, Colorado
Dooling RJ, Popper AN (2007) The effects of highway noise on birds. Report prepared for the California Department of Transportation, Division of Environmental Analysis under Contract # 43A0139
Dooling RJ, Saunders JC (1975) Hearing in the parakeet (Melopsittacus undulatus): absolute thresholds, critical ratios, frequency difference limens, and vocalizations. J Comp Physiol Psych 88(1):1–20
Dooling RJ, Mulligan JA, Miller JD (1971) Auditory sensitivity and song spectrum of the common canary (Serinus canarius). J Acoust Soc Am 50:700–709
Dooling RJ, Lohr B, Dent ML (2000) Hearing in birds and reptiles. In: Dooling RJ, Popper AN, Fay RR (eds) Comparative hearing: Birds and reptiles. Springer, New York, pp 308–359
Gall MD, Brierley LE, Lucas JR (2011) Species and sex effects on auditory processing in brown-headed cowbirds and red-winged blackbirds. Anim Behav 81(5):973–982
Gleich O, Dooling RJ, Manley GA (2005) Audiogram, body mass, and basilar papilla length: correlations in birds and predictions for extinct archosaurs. Naturwissenschaften 92:595–598
Gorga MP, Kaminski JR, Beauchaine KA, Jesteadt W (1988) Auditory brainstem responses to tone bursts in normally hearing subjects. J Speech Lang Hear R 31:87–97
Goudie R, Gregory I, Robertson J, Reed A (2000) Common eider (Somateria mollissima). Birds of North America Online. http://bna.birds.cornell.edu.proxy-um.researchport.umd.edu/bna/species/546. Accessed 10 Mar 2014
Greene CR Jr (1995) Ambient noise. In: Richardson WJ, Green CR Jr, Malme CI, Thomson DH (eds) Marine mammals and noise. Academic Press, London, pp 87–100
Guillemette M, Himmelman JH, Barette C (1993) Habitat selection by common eiders in winter and its interaction with flock size. Can J Zool 71:1259–1266
Hall JW (1992) Handbook of auditory evoked responses. Allyn & Bacon, Boston
Heffner RS, Heffner HE (1982) Hearing in the elephant (Elephas maximus): absolute sensitivity, frequency discrimination, and sound localization. J Comp Physiol Psych 96(6):926–944
Henry KS, Lucas JR (2008) Coevolution of auditory sensitivity and temporal resolution with acoustic signal space in three songbirds. Anim Behav 76:1659–1671
Henry KS, Lucas JR (2010) Auditory sensitivity and the frequency selectivity of auditory filters in the Carolina chickadee. Poecile carolinensis. Anim Behav 80(3):497–507
Houser DS, Finneran JJ (2006) A comparison of underwater hearing sensitivity in bottlenose dolphins (Tursiops truncatus) determined by eletrophysiological and behavioral methods. J Acoust Soc Am 120(3):1713–1722
Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, Ho SYW et al (2014) Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346(6215):1320–1331
Jones IL, Falls JB, Gaston AJ (1987) Vocal recognition between parent and young of ancient murrelets, Synthliboramphus antiquus (Aves: alcidae). Anim Behav 35:1405–1415
Jouventin P (1982) Visual and vocal signals in penguins, their evolution and adaptive characters. Adv Ethol 24:1–149
Kastelein RA, Dubbeldam JL, de Bakker MAG, Gerrits NM (1996) The anatomy of the walrus head (Odobenus rosmarus) Part 4: The ears and their function in aerial and underwater hearing. Aquat Mamm 22(2):95–125
Katayama A (1985) Postnatal development of auditory function in the chicken revealed by auditory brain-stem responses (ABRs). Electroencephalogr Clin Neurophysiol 62:388–398
Kettembeil S, Manley GA, Siegl E (1995) Distortion-product otoacoustic emissions and their anaesthesia sensitivity in the European starling and the chicken. Hear Res 86(1–2):47–62
Konishi M (1970) Comparative neurophysiological studies of hearing and vocalization in songbirds. Z Vergl Physiol 66:257–272
Köppl C, Gleich O (2007) Evoked cochlear potentials in the barn owl. J Comp Physiol A 193(6):601–612
Köppl C, Manley GA, Johnstone BM (1990) Peripheral auditory processing in the bobtail lizard Tiliqua rugosa. V, Seasonal effects of anaesthesia. J Comp Physiol 167(1):139–144
Ladich F, Bass AH (2003) Underwater sound generation and acoustic reception in fishes with some notes on frogs. In: Collin SP, Marshall NJ (eds) Sensory processing in aquatic environments. Springer, New York, pp 173–193
Lengagne T, Aubin T, Jouventin P, Lauga J (2000) Perceptual salience of individually distinctive features in the calls of adult king penguins. J Acoust Soc Am 107:508–516
Lohr B, Brittan-Powell EF, Dooling RJ (2013) Auditory brainstem response and auditory thresholds in woodpeckers. J Acoust Soc Am 133(1):337–342
Long GR, Schnitzler HU (1975) Behavioural audiograms from the bat, Rhinolophus ferrumequinum. J Comp Physiol 100:211–219
Machin KL (2004) Waterfowl anesthesia. Semin Avian Exot Pet 13(4):206–212
Machin KL, Caulkett NA (1998) Effects of injectable anesthetics in mallard ducks (Anas platyrhynchos): a descriptive study. J Avian Med Surg 12:255–262
McClure CJ, Ware HE, Carlisle J, Kaltenecker G, Barber JR (2013) An experimental investigation into the effects of traffic noise on distributions of birds: avoiding the phantom road. Proc Roy Sci B 280(1773):20132290
McConnell SO, Schilt MP, Dworski JG (1992) Ambient noise measurements from 100 Hz to 80 kHz in an Alaskan fjord. J Acoust Soc Am 91:1990–2003
Megela-Simmons A, Moss CF, Daniel KM (1985) Behavioral audiograms of the bullfrog (Rana catesbeiana) and the green tree frog (Hyla cinerea). J Acoust Soc Am 78:1236
Meir JU, Stockard TK, Williams CL, Ponganis KV, Ponganis PJ (2008) Heart rate regulation and extreme bradycardia in diving emperor penguins. J Exp Biol 211:1169–1179
Mowbray TB (2002) Northern gannet (Morus bassanus). Birds of North America Online. http://bna.birds.cornell.edu.proxyum.researchport.umd.edu/bna/species/693. doi:10.2173/bna.693. Accessed 10 Mar 2014
Naguib M, van Oers K, Braakhuis A, Griffioen M, de Goede P, Waas JR (2013) Noise annoys: effects of noise on breeding great tits depend on personality but not on noise characteristics. Anim Behav 85(5):949–956
Nelson JB (1978) The gannet. Buteo Books, Vermillion
Neuweiler G, Bruns V, Schuller G (1980) Ears adapted for the detection of motion, or how echolocating bats have exploited the capacities of the mammalian auditory system. J Acoust Soc Am 68:741
Nystuen JA (1986) Rainfall measurements using underwater ambient noise. J Acoust Soc Am 79:972–981
Payne KB, Langbauer WR, Thomas EM (1986) Infrasonic calls of the Asian elephant (Elephas maximus). Behav Ecol Sociobiol 18:297–301
Popper AN (1980) Scanning electron microscopic studies of the sacculus and lagena in several deep-sea fishes. Am J Anat 157:115–136
Ramprashad F, Money KE, Ronald K (1972) The harp seal, Pagophilus groenlandicus (Erxlebel, 1777). XXI. The structure of the vestibular apparatus. Can J Zool 50:1357–1361
Reijnen R, Foppen RUUD (2006) Impact of road traffic on breeding bird populations. The ecology of transportation: managing mobility for the environment. Springer, Netherlands, Netherlands, pp 255–274
Reppening CA (1972) Underwater hearing in seals: functional morphology. In: Harrison RJ (ed) Functional anatomy of marine mammals. Academic Press, London, pp 307–331
Reubhausen MR, Brozoski TJ, Bauer CA (2012) A comparison of the effects of isofluorane and ketamine anesthesia on auditory brainstem response (ABR) thresholds in rats. Hear Res 287(1–2):25–29
Rijke AM (1970) Wettability and phylogenetic development of feather structure in water birds. J Exp Biol 52(2):469–479
Robertson GJ, Goudie RI (1999) Harlequin duck (Histrionicus histrionicus). Birds of North America Online. http://bna.birds.cornell.edu.proxy-um.researchport.umd.edu/bna/species/466. Accessed 10 Mar 2014
Robertson GJ, Savard JPL (2002) Long-tailed duck (Clangula hyemalis). Birds of North America Online: http://bna.birds.cornell.edu.proxy-um.researchport.umd.edu/bna/species/651 doi:10.2173/bna.651. Accessed 10 Mar 2014
Sadè J, Handrich Y, Bernheim J, Cohen D (2008) Pressure equilibration in the penguin middle ear. Acta Otolaryngol 128:18–21
Savard JPL, Bordage D, Reed A (1998) Surf scoter (Melanitta perspicillata). Birds of North America Online: http://bna.birds.cornell.edu.proxy-um.researchport.umd.edu/bna/species/651 doi:10.2173/bna.651. Accessed 10 Mar 2014
Sea Duck Joint Venture (2012) Atlantic and Great Lakes sea duck migration study. Progress Report. http://seaduckjv.org/atlantic_migration_study/atlantic_grlakes_sea_duck_rpt_november2012_compressed.pdf. Accessed 24 Feb 2014
Slabbekoorn H (2013) Songs of the city: noise-dependent spectral plasticity in the acoustic phenotype of urban birds. Anim Behav 85:1089–1099
Sladen WL, Leresche RE (1970) New and developing techniques in Antarctic ornithology. Antarct Ecol 1:585–596
Stenfors LE, Sadè J, Hellström S, Anniko M, Folkow L (2000) Exostoses and cavernous venous formation in the external auditory canal of the hooded seal as a functional physiological organ. Acta Otolaryngol 120(8):940–943
Trainer JE (1946) The auditory acuity of certain birds. Doctoral dissertation, Cornell University. In: Fay RR (ed) (1988) Hearing in vertebrates: A psychological databook. Hill-Fay Associates, Winnetka, IL
Urick RJ (1983) The noise background of the sea: ambient noise level. In: Urick RJ (ed) Principles of underwater sound. Peninsula Publishing, Los Altos, pp 202–236
Welsch U, Riedelsheimer B (1997) Histophysiological observations on the external auditory meatus, middle, and inner ear of the Weddell seal (Leptonychotes weddelli). J Morphol 234(1):25–36
Wenz GM (1962) Acoustic ambient noise in the ocean: spectra and sources. J Acoust Soc Am 34:1936–1956
Wever EG, Herman PN, Simmons JA, Hertzler DR (1969) Hearing in the blackfooted penguin, Spheniscus demersus, as represented by the cochlear potentials. Proc Natl Acad Sci USA 63:676–680
Wilson RP, Culik B, Danfeld R, Adelung D (1991) People in Antarctica—how much do Adelie Penguins Pygoscelis adeliae care? Polar Biol 11:363–379
Wolski LF, Anderson RC, Bowles AE, Yochem PK (2003) Measuring hearing in the harbor seal (Phoca vitulina): comparison of behavioral and auditory brainstem response techniques. J Acoust Soc Am 113(1):629–637
Woolley SMN, Rubel EW (1999) High-frequency auditory feedback is not required for adult song maintenance in Bengalese finches. J Neurosci 19(1):358–371
Yuen MM, Nachtigall PE, Breese M, Supin AY (2005) Behavioral and auditory evoked potential audiograms of a false killer whale (Pseudorca crassidens). J Acoust Soc Am 118(4):2688–2695
Acknowledgments
The Animal Care and Use Committees at both the University of Maryland and the U.S. Geological Survey Patuxent Wildlife Research Center (where the birds were housed and tested) approved all of the following procedures. We thank Edward Smith for the use of his software, Elizabeth Brittan-Powell for her training on ABR procedures, and Arthur Popper for his editing. Funding for this project was provided by several sources: National Institutes of Health (NIH) DC00436 to Catherine Carr, NIH P30 DC0466 to the University of Maryland Center for Comparative and Evolutionary Biology of Hearing, by training grant DC-000466 from the National Institute of Deafness and Communicative Disorders of the National Institutes of Health, and from U.S. Geological Survey Patuxent Wildlife Research Center.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Crowell, S.E., Wells-Berlin, A.M., Carr, C.E. et al. A comparison of auditory brainstem responses across diving bird species. J Comp Physiol A 201, 803–815 (2015). https://doi.org/10.1007/s00359-015-1024-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-015-1024-5