Journal of Comparative Physiology A

, Volume 203, Issue 2, pp 121–132 | Cite as

Precocious hearing in harbour porpoise neonates

  • Magnus WahlbergEmail author
  • Lara Delgado-García
  • Jakob H. Kristensen
Original Paper


Hearing is the primary sensory modality for toothed whales, but it is not known at which age it is fully developed. For newborn calves, hearing could fill an important function in maintaining contact with the mother and to develop echolocation skills. We non-invasively measured the auditory brainstem response (ABR) in two neonate (age 1–4 days) and three adult harbour porpoises (Phocoena phocoena). The stimuli consisted of clicks centred at 130 kHz, which is within the frequency band used for echolocation and communication in this species. The temporal pattern of the neonate ABRs was indistinguishable to the adult ones. There were no significant differences between calves and adults regarding hearing thresholds and ABR latencies. The ABR amplitudes were up to more than an order of magnitude larger in newborns than in adults, most likely due to the neonates’ smaller size. These results indicate that hearing is fully developed within a day after birth, which suggests that harbour porpoise neonates have the earliest hearing development of any mammal studied so far. This may be explained by the evolutionary pressures imposed by the aquatic environment for a rapid development of the key sensory system in harbour porpoises.


Toothed whale hearing Auditory brainstem response Hearing development Biosonar Underwater hearing 



The experiments were performed according to the ethical rules of Danish Council for Experiments on Animals. The animals are held at the Fjord&Bælt under a contract of the Danish Nature Agency, Ministry of Environment and Food of Denmark, We thank all the trainers and volunteers helping out with observing the calf and preparing for the ABR trials, and Kristian Beedholm for valuable comments on an earlier version of this paper. This project was funded by grants from the Danish National Research Council to Peter Madsen, Annemarie Surlykke, and Magnus Wahlberg.


  1. Aitkin LM, Moore DR (1975) Inferior colliculus. II. Development of tuning characteristics and tonotopic organization in central nucleus of the neonatal cat. J Neurophysiol 38(5):1208–1216PubMedGoogle Scholar
  2. Au WWL, Hastings MC (2008) Principles of marine bioacoustics. Chapman Hall, New YorkCrossRefGoogle Scholar
  3. Blatchley BJ, Cooper WA, Coleman JR (1987) Development of auditory brainstem response to tone pip stimuli in the rat. Dev. Brain Res 32:75–84CrossRefGoogle Scholar
  4. Bradbury JW, Vehrencamp SL (2011) Principles of animal communication. Sinauer Associates, New YorkGoogle Scholar
  5. Brandt C, Malmkvist J, Nielsen RL, Brande-Lavridsen N, Surlykke A (2013) Development of vocalization and hearing in American mink (Neovison, vison). J Exp Biol 216:3542–3550CrossRefPubMedGoogle Scholar
  6. Clausen KT, Wahlberg M, Beedholm K, Madsen PT (2010) Click communication in harbour porpoises Phocoena phocoena. Bioacoustics 20:1–28CrossRefGoogle Scholar
  7. Corey DP, Breakefield XO (1994) Transcription factors in inner ear development. Proc Natl Acad Sci USA 91:433–436CrossRefPubMedPubMedCentralGoogle Scholar
  8. Derrickson EM (1992) Comparative reproductive strategies of altricial and precocial eutherian mammals. Funct Ecol 6:57–65CrossRefGoogle Scholar
  9. Dum N (1984) Postnatal development of the auditory evoked brainstem potentials in the Guinea pig. Acta Oto-laryngol 97:63–68CrossRefGoogle Scholar
  10. Eggermont JJ, Moore JK (2012) Morphological and functional development of the auditory nervous system. In: Werner L, Fay RR, Popper AN (eds) Springer handbook of auditory research, Vo. 42, human auditory development. Springer-Verlag, New York, pp 61–105Google Scholar
  11. Fabiani M, Sohmer H, Tait C, Gafni M, Kinarti B (1979) A functional measure of brain activity: brain stem transmission time. Electroen Clin Neuro 47:483–491CrossRefGoogle Scholar
  12. Fritzsch B, Barald KF, Lomax MI (1997) Early embryology of the vertebrate ear. In: Werner L, Fay RR, Popper AN (eds) Springer Handbook of Auditory Research, Vo. 42, Human auditory development. Springer-Verlag, New York, pp 80–145Google Scholar
  13. Galatius A, Andersen MBER, Haugan B, Langhoff HE, Jespersen A (2006) Timing of epiphyseal development in the flipper skeleton of the harbour porpoise (Phocoena phocoena) as an indicator of paedomorphosis. Acta Zool-Stockholm 87:77–82Google Scholar
  14. Geal-Dor M, Freeman S, Li G, Sohmer H (1993) Development of hearing in neonatal rats: air and bone conducted ABR thresholds. Hearing Res 69(1–2):236–242CrossRefGoogle Scholar
  15. Gorga MP, Kaminski JR, Beauchaine KA, Jesteadt W (1988) Auditory brainstem response to tone bursts in normally hearing subjects. J Speech Hear Res 31:87–97CrossRefPubMedGoogle Scholar
  16. Grossman C (1955) Eletro-ontogenesis of celebral activity. Arch Neuro Psychiatr 74(2):186–202Google Scholar
  17. Hecox K, Galambos R (1974) Brain stem auditory evoked responses in human infants and adults. Arch Otolaryngol 99:30–33CrossRefPubMedGoogle Scholar
  18. Houser DS, Finneran JJ (2006) Variation in the hearing sensitivity of a dolphin population determined through the use of evoked potential audiometry. J Acoust Soc Am 120(6):4090–4099CrossRefPubMedGoogle Scholar
  19. Jamon M (2006) The early development of motor control in neonate rat. C R Pale 5:657–666CrossRefGoogle Scholar
  20. Kastelein RA, Hoek L, de Jong CAF, Wensveen PJ (2010) The effect of signal duration on the underwater detection thresholds of a harbour porpoise (Phocoena phocoena) for single frequency-modulated tonal signals between 0.25 and 160 kHz. J Acoust Soc Am 128(5):3211–3222CrossRefPubMedGoogle Scholar
  21. Lancaster WC, Ary WJ, Krysl P, Cranford TW (2015) Precocial development within the tympanoperiotic complex in cetaceans. Mar Mammal Sci 31(1):369–375CrossRefGoogle Scholar
  22. Linnenschmidt M, Wahlberg M, Damsgaard Hansen J (2013) Modulation rate transfer function of a harbour porpoise (Phocoena phocoena). J Comp Physiol B 199(2):115–126CrossRefGoogle Scholar
  23. Liu GB (2003) Functional development of the auditory brainstem in the tammar wallaby (Macropus eugenii): the superior olivary complex and its relationship with the auditory brainstem response (ABR). Hearing Res 175:152–164CrossRefGoogle Scholar
  24. Lyamin O, Pryaslova J, Lance V, Siegel J (2005) Animal behaviour: Continuous activity in cetaceans after birth. Nature 435:1177CrossRefPubMedGoogle Scholar
  25. Madsen PTM, Wahlberg M (2007). Recording and quantification of ultrasonic echolocation clicks from free-ranging toothed whales. Deep-Sea Res Pt I 54(8):1421–1444CrossRefGoogle Scholar
  26. Møhl B, Andersen S (1973) Echolocation: high-frequency component in the click of the harbour porpoise (Phocoena ph. L.). J Acoust Soc Am 54:1368–1372CrossRefPubMedGoogle Scholar
  27. Mooney TA, Nachtigall PE, Yuen MML (2006) Temporal resolution of the Risso’s dolphin, Grampus griseus, auditory system. J Comp Physiol A 192:373–380CrossRefGoogle Scholar
  28. Mooney TA, Yamato M, Branstetter BK (2012) Hearing in cetaceans: from natural history to experimental biology. Adv Mar Biol 63:197–244CrossRefPubMedGoogle Scholar
  29. Moore JK, Perazzo LM, Braun A (1995) Time course of axonal myelination in the human brainstem auditory pathway. Hearing Res 87:21–31CrossRefGoogle Scholar
  30. Nachtigall PE, Yen MML, Mooney TA, Taylor KA (2005) Hearing measurements from a stranded infant Risso’s dolphin, Grampus griseus. J Exp Biol 208:4181–4188CrossRefPubMedGoogle Scholar
  31. Noren SR, Noren DP, Gaydos JK (2015) Living in the fast lane: rapid development of the locomotor muscle in immature harbor porpoises (Phocoena phocoena). J Comp Physiol B 184:1065–1076CrossRefGoogle Scholar
  32. Popov VV, Supin A Ya (1990) Auditory brain stem responses in characterization of dolphin hearing. J Comp Physiol A 166:385–393CrossRefPubMedGoogle Scholar
  33. Pujol R, Hilding D (1973) Anatomy and physiology of the onset of auditory function. Acta Oto-laryngol 76:1–10CrossRefGoogle Scholar
  34. Read AJ (1999) Harbour porpoise—Phocoena phocoena (Linnaeus, 1758). In: Ridgway SH, Harrison SR (eds) Handbook of Marine Mammals vol 6: The second book of dolphins and porpoises. Academic Press, New York, pp 323–356Google Scholar
  35. Ridgway SH, Carder DA (2001) Assessing hearing and sound production in cetaceans not available for behavioural audiograms: experiences with sperm, pygmy sperm and gray whales. Aq Mamm 27:267–276Google Scholar
  36. Ridgway SH, Bullock TH, Carder DA, Seeley RL, Woods D, Galambos R (1981) Auditory brainstem response in dolphins. Proc Nat Acad Sci USA 78(3):1943–1947CrossRefPubMedPubMedCentralGoogle Scholar
  37. Shipley C, Buchwald JS, Norman R, Guthrie D (1980) Brain stem auditory evoked response development in the kitten. Brain Res 182:313–326CrossRefPubMedGoogle Scholar
  38. Siebert U, Pozniak B, Andersen Hansen K, Nordstrom G, Teilmann J, van Elk N, Vossen A, Dietz R (2011) Investigations of thyroid and stress hormones in free-ranging and captive harbour porpoises (Phocoena phocoena): a pilot study. Aq Mamm 37(4):443–453CrossRefGoogle Scholar
  39. Sininger YS, Abdala C, Cone-Wesson B (1997) Auditory threshold sensitivity of the human neonate as measured by the auditory brainstem response. Hearing Res 104:27–38CrossRefGoogle Scholar
  40. Smith DJ, Kraus N (1987) Postnatal development of the auditory brainstem response (ABR) in the unanesthetized gerbil. Hearing Res 27:157–164CrossRefGoogle Scholar
  41. Starr A, Amlie RN, Martin WH, Sanders S (1977) Development of auditory function in newborn infants revealed by auditory brainstem potentials. Pediatrics 60:831–839PubMedGoogle Scholar
  42. Sterbing SJ (2002) Postnatal development of vocalizations and hearing in the phyllostomid bat, Carollia perspicillata. J Mammal 83(2):516–525CrossRefGoogle Scholar
  43. Sterbing SJ, Schmidt U, Rübsamen R (1994) Postnatal development of frequency-place code and tuning characteristics in the auditory midbrain of the phyllostomid bat Carollia perspicillata. Hearing Res 76:133–146CrossRefGoogle Scholar
  44. Supin AY, Popov VV, Mass AM (2001) The sensory physiology of aquatic mammals. Kluwer Academic Publishers, BostonCrossRefGoogle Scholar
  45. Szymanski MD, Supin A Ya, Bain DE (1998) Killer whale (Orcinus orca) auditory evoked potentials to rhythmic clicks. Mar Mammal Sci 14(4):676–691CrossRefGoogle Scholar
  46. Walsh EJ, McGee J, Javel E (1986a) Development of auditory-evoked potentials in the cat. I. Onset of response and development of sensitivity. J Acoust Soc Am 79(3):712–723Google Scholar
  47. Walsh EJ, McGee J, Javel E (1986b) Development of auditory-evoked potentials in the cat. II. Wave latencies. J Acoust Soc Am 79(3):725–744Google Scholar
  48. Werner LA, Gray L (1997) Behavioral studies of hearing development. In: Werner L, Fay RR, Popper AN (eds) Springer handbook of auditory research, Vo. 42, Human auditory development. Springer-Verlag, New York, pp 12–79Google Scholar
  49. West KL, Ramer J, Brown JL, Sweeney J, Hanahoe EM, Reidarson T, Proudfoot J, Bergfelt DR (2014) Thyroid hormone concentrations in relation to age, sex, pregnancy, and perinatal loss in bottlenose dolphins (Tursiops truncates). Gen Comp Endocrinol 197:73–81CrossRefPubMedGoogle Scholar
  50. Wilkinson AR, Jiang ZD (2006) Brainstem auditory evoked response in neonatal neurology. Seminarion Fetal Neonatal. Medicine (Baltimore) 11:444–451Google Scholar
  51. Zar JH (1996) Biostatistical analysis. 3rd edn. Prentice-Hall International, Inc., Upper Saddle RiverGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Biology, Marine Biological Research CentreUniversity of Southern DenmarkKertemindeDenmark
  2. 2.Fjord&BæltKertemindeDenmark

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