Environmental Biology of Fishes

, Volume 95, Issue 2, pp 275–290 | Cite as

Development of the ear, hearing capabilities and laterophysic connection in the spotfin butterflyfish (Chaetodon ocellatus)

  • Jacqueline F. Webb
  • Ryan M. Walsh
  • Brandon M. Casper
  • David A. Mann
  • Natasha Kelly
  • Nicole Cicchino


The ontogeny of the ear, swim bladder and laterophysic connection was investigated in the spotfin butterflyfish, Chaetodon ocellatus in order to determine how the development of the laterophysic connection (a Chaetodon synapomorphy) is correlated with ontogenetic changes in the hearing capabilities in these abundant and ecologically important coral reef fishes. Histological and cleared and stained material revealed that the medial opening in the lateral line canal in the supracleithrum (which defines the laterophysic connection), an inflated physoclistous swim bladder, and the three otolithic organs are already present in the smallest individuals examined (7–15 mm SL). The medial opening in the supracleithrum increases in size and the cylindrical swim bladder horns form after the loss of the head plates characteristic of the tholichthys stage, in individuals ≥29 mm SL. The three sensory maculae of the ear increase in size, and the shape of the sacculus changes most dramatically with fish growth; hair cell density is highest in the utriculus. Physiological analysis of the reponse to sound pressure showed that larval and juvenile C. ocellatus had a hearing sensitivity peak at 100–200 Hz, which was ~30–40 dB more sensitive than that measured in larval coral reef fishes (e.g., damselfishes) that lack swim bladder horns. C. ocellatus did not show any ontogenetic changes in sensitivity to sound pressure, which may be explained by the fact that the growth of the swim bladder horns maintains the small distance between the swim bladder and ear that was established earlier during the larval stage. The timing of the development of the swim bladder horns suggests that if the laterophysic connection has a sensory acoustic function, its presence in individuals >29 mm SL suggests that its role is limited to post-settlement, reef-based behaviors.


Swim bladder Lateral line Hearing AEP Sensory ontogeny Ear Laterophysic connection 



We thank Ken Able (Rutgers University Marine Field Station, Tuckerton, NJ) for providing the specimens used in this study, and for providing the lab space in which our physiological analysis was carried out. Karsten Hartel (Museum of Comparative Zoology, Harvard University) provided a gift of small Chaetodon larvae for histological analysis. Jeff Leis (Australian Museum, Sydney) provided fruitful discussions and read an earlier draft of this manuscript. The histological analysis of ear development constituted a Senior Undergraduate Thesis by RMW. An HHMI Undergraduate Education grant to Villanova University provided support for NK and NC. This work was carried out under an approved Villanova University IACUC protocol. It was supported by a Villanova Faculty Summer Research Grant and NSF grants IOS-9603896 and IOS-0132607 to JFW.


  1. Able KW, Fahay MP (1998) The first year in the life of estuarine fishes in the middle Atlantic bight. Rutgers University Press, New BrunswickGoogle Scholar
  2. Allen JM, Blaxter JHS, Denton EJ (1976) The functional anatomy and development of the swim bladder-inner ear-lateral line system in herring and sprat. J Mar Biol Assoc UK 56:471–486CrossRefGoogle Scholar
  3. Atema J, Kingsford MJ, Gerlach G (2002) Larval reef fish could use odour for detection, retention and orientation to reefs. Mar Ecol Prog Ser 241:151–160CrossRefGoogle Scholar
  4. Bauchot R, Thomas A, Bauchot M-L (1989) The membranous labyrinth and its innervation in Chaetodon trifasciatus (Pisces, Teleostei, Chaetodontidae). Environ Biol Fish 25:235–242CrossRefGoogle Scholar
  5. Blaxter JHS, Hoss DE (1981) Startle response in herring: the effect of sound stimulus frequency, size of fish and selective interference with the acoustico-lateralis system. J Mar Biol Assoc UK 61:871–879CrossRefGoogle Scholar
  6. Boyle KS, Tricas TC (2006a) Acoustic communication by butterflyfishes (Chaetodontidae) on noisy coral reefs. Amer Geophys Union, Annual Meeting. Abstract #OS440-02. www.agu.org/meetings/os06/os06-sessions/os06_OS44O.htm
  7. Boyle KS, Tricas TC (2006b) Sound communication by the forceps fish, Forcipiger flavissimus (Chaetodontidae). J Acoust Soc Am 120:3104Google Scholar
  8. Boyle KS, Tricas TC (2010) Pulse sound generation, anterior swim bladder buckling, and associated muscle activity in the pyramid butterflyfish, Hemitaurichthys polylepis. J Exper Biol 213:3881–3893CrossRefGoogle Scholar
  9. Braun CB, Grande T (2008) Evolution of peripheral mechanisms for the enhancement of sound reception. In: Webb JF, Fay RR, Popper AN (eds) Fish bioacoustics. Springer, NY, pp 99–144CrossRefGoogle Scholar
  10. Dudley B, Tolimieri M, Montgomery J (2000) Swimming ability of the larvae of some reef fishes from New Zealand waters. Mar Freshw Res 51:783–787CrossRefGoogle Scholar
  11. Egner SA, Mann DA (2005) Auditory sensitivity of sergeant major damselfish (Abudefduf saxatilis) from post-settlement juvenile to adult. Mar Ecol Prog Ser 285:213–222CrossRefGoogle Scholar
  12. Fay RR, Popper AN, Webb JF (2008) Introduction to fish bioacoustics. In: Webb JF, Fay RR, Popper AN (eds) Fish bioacoustics. Springer, NY, pp 1–15CrossRefGoogle Scholar
  13. Higgs DM, Rollo AK, Souza MJ, Popper AN (2003) Development of form and function in peripheral auditory structures of the zebrafish (Danio rerio). J Acoust Soc Am 113:1145–1154PubMedCrossRefGoogle Scholar
  14. Higgs DM, Plachta DTT, Rollo AK, Singheiser M, Hastings MC, Popper AN (2004) Development of ultrasound detection in American shad (Alosa sapidissima). J Exper Biol 207:155–163CrossRefGoogle Scholar
  15. Hoss DE, Blaxter JHS (1982) Development and function of the swim bladder-inner ear-lateral line system in the Atlantic menhaden, Brevoortia tyrannus (Latrobe). J Fish Biol 20:131–142CrossRefGoogle Scholar
  16. Kenyon TN (1995) Ontogenetic changes in the auditory sensitivity of the bicolor damselfish, Pomacentrus partitus. Unpubl. PhD. Dissertation, University of Miami, Miami, FLGoogle Scholar
  17. Kenyon TN (1996) Ontogenetic changes in the auditory sensitivity of damselfishes (Pomacentridae). J Comp Physiol A 179:553–561CrossRefGoogle Scholar
  18. Kenyon TN, Ladich F, Yan HY (1998) A comparative study of hearing ability in fishes; the auditory brainstem response approach. J Comp Physiol A 182:307–318PubMedCrossRefGoogle Scholar
  19. Lecchini D, Shima J, Banaigs B, Galzin R (2005) Larval sensory abilities and mechanisms of habitat selection of a coral reef fish during settlement. Oecologia 143:326–334PubMedCrossRefGoogle Scholar
  20. Leis JM (2011) How Nemo finds home: the neuroecology of dispersal and of population connectivity in larvae of marine fishes. Integr Comp Biol 51(5):826–843Google Scholar
  21. Leis JM, Carson-Ewart BM (1997) In situ swimming speeds of the late pelagic larvae of some Indo-Pacific coral-reef fishes. Mar Ecol Prog Ser 159:165–174CrossRefGoogle Scholar
  22. Leis JM, Carson-Ewart BM (1999) In situ swimming and settlement behaviour of larvae of an Indo-Pacific coral-reef fish, the coral trout (Pisces, Serranidae, Plectropomus leopardus). Mar Biol 134:51–64CrossRefGoogle Scholar
  23. Leis JM, Carson-Ewart BM (2003) Orientation of pelagic larvae of coral-reef fishes in the ocean. Mar Ecol Prog Ser 252:239–253CrossRefGoogle Scholar
  24. Leis JM, Carson-Ewart BM, Cato DH (2002) Sound detection in situ by the larvae of a coral-reef damselfish (Pomacentridae). Mar Ecol Prog Ser 232:259–268CrossRefGoogle Scholar
  25. Leis JM, Hay AC, Lockett MM, Chen J-P, Fang L-S (2007a) Ontogeny of swimming speed in larvae of pelagic-spawning, tropical, marine fishes. Mar Ecol Prog Ser 349:257–269CrossRefGoogle Scholar
  26. Leis JM, Lockett MM (2005) Localization of reef sounds by settlement-stage larvae of coral-reef fishes (Pomacentridae). Bull Mar Sci 76:715–724Google Scholar
  27. Leis JM, Sweatman HPA, Reader SE (1996) What the pelagic stages of coral reef fishes are doing out in blue water: daytime field observations of larval behaviour. Mar Freshw Res 47:401–411CrossRefGoogle Scholar
  28. Leis JM, Wright KJ, Johnson RN (2007b) Behavior that influences dispersal and connectivity in the small, young larvae of a reef fish. Mar Biol 153:103–117CrossRefGoogle Scholar
  29. Mann DA, Higgs DM, Tavolga WN, Souza MJ, Popper AN (2001) Ultrasound detection by clupeiform fishes. J Acoust Soc Am 109:3048–3054PubMedCrossRefGoogle Scholar
  30. Mann DA, Casper BM, Boyle KS, Tricas TC (2007) On the attraction of larval fishes to reef sounds. Mar Ecol Prog Ser 338:307–310CrossRefGoogle Scholar
  31. McBride RS, Able KW (1998) Ecology and fate of butterflyfishes, Chaetodon spp. in the temperate Western North Atlantic. Bull Mar Sci 63:401–416Google Scholar
  32. Montgomery JC, Jeffs A, Simpson SD, Meekan M, Tindle C (2006) Sound as an orientation cue for the pelagic larvae of reef fishes and decapod crustaceans. Adv Mar Biol 51:143–199PubMedCrossRefGoogle Scholar
  33. O’Connell CP (1955) The swim bladder and its relation to the inner ear in Sardinops caerulea and Engraulis mordax. US Fish Bull 56:505–533Google Scholar
  34. Popper AN (1977) A scanning electron microscopic study of the sacculus and lagena in the ears of fifteen species of teleost fishes. J Morphol 153:418–497CrossRefGoogle Scholar
  35. Popper AN, Fay RR (2011) Rethinking sound detection by fishes. Hear Res 273(1–2):25–36PubMedCrossRefGoogle Scholar
  36. Pothoff T (1984) Clearing and staining technique. In: Ontogeny and systematics of fishes. Spec Publ 1, Amer Soc Ichthyol Herpetol. Allen Press, Lawrence KS, pp 35–37Google Scholar
  37. Scholik AR, Yan HY (2001) Effects of underwater noise on auditory sensitivity of a cyprinid fish. Hear Res 152:17–24PubMedCrossRefGoogle Scholar
  38. Scholik AR, Yan HY (2002) The effects of noise on the auditory sensitivity of the bluegill sunfish, Lepomis macrochirus. Comp Biochem Physiol 133A:43–52Google Scholar
  39. Simpson SD, Meekan M, Montgomery J, McCauley R, Jeffs A (2005) Homeward sound. Science 308:221PubMedCrossRefGoogle Scholar
  40. Smith WL, Webb JF, Blum SD (2003) The evolution of the laterophysic connection with a revised phylogeny and taxonomy of butterflyfishes (Teleostei: Chaetodontidae). Cladistics 19:287–306CrossRefGoogle Scholar
  41. Stobutzki IC (1997) Energetic cost of sustained swimming in the late pelagic stages of reef fishes. Mar Ecol Prog Ser 152:249–259CrossRefGoogle Scholar
  42. Sweatman H (1988) Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues. J Exper Mar Biol Ecol 124:163–174CrossRefGoogle Scholar
  43. Tolimieri N, Jeffs A, Montgomery JC (2000) Ambient sound as a cue for navigation by the pelagic larvae of reef fishes. Mar Ecol Prog Ser 207:219–224CrossRefGoogle Scholar
  44. Tolimieri N, Haine O, Jeffs A, McCauley R, Montgomery J (2004) Directional orientation of pomacentrid larvae to ambient reef sound. Coral Reefs 23:184–194Google Scholar
  45. Tricas TC, Boyle KS (2005) The evolution of pairing behavior, sound production and hearing in chaetodontid butterflyfishes: evidence from behavior and physiology. Brain Behav Evol 66:143Google Scholar
  46. Tricas TC, Boyle KS (2006) Acoustico-lateralis communication in coral reef butterflyfishes. J Acoust Soc Am 120:3104Google Scholar
  47. Tricas TC, Kajiura SM, Kosaki RK (2006) Acoustic communication in territorial butterflyfish: test of the sound production hypothesis. J Exper Biol 209:4994–5004CrossRefGoogle Scholar
  48. Webb JF (1998) Laterophysic connection: a unique link between the swim bladder and the lateral-line system in Chaetodon (Perciformes: Chaetodontidae). Copeia 1998:1032–1036CrossRefGoogle Scholar
  49. Webb JF, Smith WL (2000) The laterophysic connection in chaetodontid butterflyfish: morphological variation and speculations on sensory function. Phil Trans R Soc Lond B 355:1125–1129CrossRefGoogle Scholar
  50. Webb JF, Smith WL, Ketten DR (2006) The laterophysic connection and swim bladder in butterflyfishes in the genus Chaetodon (Perciformes: Chaetodontidae). J Morphol 267:1338–1355PubMedCrossRefGoogle Scholar
  51. Webb JF, Montgomery JC, Mogdans J (2008) Bioacoustics and the lateral line system of fishes. In: Webb JF, Fay RR, Popper AN (eds) Fish bioacoustics. Springer, NY, pp 145–182CrossRefGoogle Scholar
  52. Webb JF, Herman JL, Woods CF, Ketten DR (2010) The ears of butterflyfishes: “hearing generalists” on noisy coral reefs? J Fish Biol 77:1434–1451CrossRefGoogle Scholar
  53. Wright KJ, Higgs DM, Belanger AJ, Leis JM (2005) Auditory and olfactory abilities of pre-settlement larvae and post-settlement juveniles of a coral reef damselfish (Pisces: Pomacentridae). Mar Biol 147:1425–1434CrossRefGoogle Scholar
  54. Wright KJ, Higgs DM, Belanger AJ, Leis JM (2008) Auditory and olfactory abilities of larvae of the Indo-Pacific coral trout Plectropomus leopardus (Lacepede) at settlement. J Fish Biol 72:2543–2556CrossRefGoogle Scholar
  55. Wright KJ, Higgs DM, Cato DM, Leis JM (2010) Auditory sensitivity in settlement-stage larvae of coral reef fishes. Coral Reefs 29:235–243CrossRefGoogle Scholar
  56. Wright KJ, Higgs DM, Leis JM (2011) Ontogenetic and interspecific variation in hearing ability in marine fish larvae. Mar Ecol Prog Ser 424:1–13CrossRefGoogle Scholar
  57. Wysocki LE, Ladich F (2001) The ontogenetic development of auditory sensitivity, vocalization and acoustic communication in the labryinth fish Trichopsis vittata. J Comp Physiol A 187:177–187PubMedCrossRefGoogle Scholar
  58. Zeddies DG, Fay RR (2005) Development of the acoustically evoked behavioral response in zebrafish to pure tones. J Exper Biol 208:1363–1372Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Jacqueline F. Webb
    • 1
    • 2
  • Ryan M. Walsh
    • 2
  • Brandon M. Casper
    • 3
    • 4
  • David A. Mann
    • 3
  • Natasha Kelly
    • 2
  • Nicole Cicchino
    • 2
  1. 1.Department of Biological SciencesUniversity of Rhode IslandKingstonUSA
  2. 2.Department of BiologyVillanova UniversityVillanovaUSA
  3. 3.College of Marine ScienceUniversity of South FloridaSt. PetersburgUSA
  4. 4.Department of BiologyUniversity of MarylandCollege ParkUSA

Personalised recommendations