Auditory and olfactory abilities of pre-settlement larvae and post-settlement juveniles of a coral reef damselfish (Pisces: Pomacentridae)

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Abstract

The propagules of most species of reef fish are advected from the reef, necessitating a return to reef habitats at the end of the pelagic stage. There is increasing evidence of active attraction to the reef but the sensory abilities of reef fish larvae have not been characterized well enough to fully identify cues. The electrophysiological methods of auditory brainstem response (ABR) and electroolfactogram (EOG) were used to investigate auditory and olfactory abilities of pre- and post-settlement stages of a damselfish, Pomacentrus nagasakiensis (Pisces, Pomacentridae). Audiograms of the two ontogenetic stages were similar. Pre-settlement larvae heard as well as their post-settlement counterparts at all but two of the tested frequencies between 100 Hz and 2,000 Hz. At 100 and 600 Hz, pre-settlement larvae had ABR thresholds 8 dB higher than those of post-settlement juveniles. Both stages were able to detect locally recorded reef sounds. Similarly, no difference in olfactory ability was found between the two ontogenetic stages. Both stages showed olfactory responses to conspecifics as well as L-alanine. Therefore, the auditory and olfactory senses have similar capabilities in both ontogenetic stages. Settlement stage larvae of P. nagasakiensis can hear and smell reef cues but it is unclear as to what extent larvae use these sounds or smells, or both, as cues for locating settlement sites.

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References

  1. Allen GR (1991) Damselfishes of the World. Mergus Publishers, Melle

    Google Scholar 

  2. Arvedlund M, McCormick MI, Fautin DG, Bildsoe M (1999) Host recognition and possible imprinting in the anemonefish Amphiprion melanopus (Pisces: Pomacentridae). Mar Ecol Prog Ser 188:207–218

    Article  Google Scholar 

  3. Arvedlund M, Neilson LE (1996) Do the anemonefish Amphiprion ocellaris (Pisces: Pomacentridae) imprint themselves to their host sea anemone Heteractis magnifica (Anthozoa: Actinidae)? Ethology 102:197–211

    Article  Google Scholar 

  4. Atema J, Kingsford MJ, Gerlach G (2002) Larval reef fish could use odour for detection, retention and orientation to reefs. Mar Ecol Prog Ser 241:151–160

    Article  Google Scholar 

  5. Belanger AJ, Arbuckle WJ, Corkum LD, Gammon DB, Li W, Scott AP, Zeilinski BS (2005) Behavioral and electrophysiological responses by reproductive female round gobies (Neogobius melanostomus) to odours released by conspecific males. J Fish Biol (submitted)

  6. Caprio J (1978) Olfaction and taste in the channel catfish: an electrophysiological study of the responses to amino acids and derivatives. J Comp Physiol A 123:357–371

    Article  Google Scholar 

  7. Carr WES, Blumenthal KM, Netherton JC (1977) Chemoreception in the pigfish, Orthopristis chrysopterus: the contribution of amino acids and betaine to stimulation of feeding behaviour by various extracts. Comp Biochem Physiol A 58:69–73

    Article  CAS  Google Scholar 

  8. Cato DH (1978) Marine biological choruses observed in tropical waters near Australia. J Acoust Soc Am 64:736–743

    Article  Google Scholar 

  9. Corwin JT (1983) Postembryonic growth of the macula neglecta auditory detector in the ray, Raja clavata: Continual increases in hair cell number, neural convergence, and physiological sensitivity. J Comp Neurol 217:345–356

    Article  PubMed  CAS  Google Scholar 

  10. Corwin JT, Bullock TH, Schweitzer J (1982) The auditory brainstem response in five vertebrate classses. Electroen Clin Neuro 54:629–641

    Article  CAS  Google Scholar 

  11. Egner SA, Mann D (2005) Auditory sensitivity of sergeant major damselfish Abudefduf saxatilis from post-settlement juvenile to adult. Mar Ecol Prog Ser 285:213–222

    Article  Google Scholar 

  12. Elliot J, Elliot JM, Mariscal RN (1995) Host selection, location, and association behaviors of anemonefishes in field settlement experiments. Mar Biol 122:377–389

    Article  Google Scholar 

  13. Fay RR, Megala Simmons A (1999) The sense of hearing in fishes and amphibians. In: Fay RR, Popper AN (eds) Comparative hearing: fish and amphibians. Springer, Berlin Heidelberg New York, pp 269–318

    Google Scholar 

  14. Gorga MP, Kaminski JR, Beauchaine KA, Jesteadt W (1988) Auditory brainstem response to tone bursts in normally hearing subjects. J Speech Hear Res 31:87–97

    PubMed  CAS  Google Scholar 

  15. Hara TJ (1992) Mechanisms of olfaction. In: Hara TJ (ed) Fish chemoreception. Chapman and Hall, London, pp 150–170

    Google Scholar 

  16. Higgs DM (2002) Development of the fish auditory system: how do changes in auditory structure affect function? Bioacoustics 12:180–182

    Google Scholar 

  17. 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 113:1145–1154

    Article  PubMed  Google Scholar 

  18. Higgs DM, Souza MJ, Wilkins HR, Presson JC, Popper AN (2002) Age- and size-related changes in the inner ear and hearing ability of the adult zebrafish (Danio rerio). J Assoc Res Otolaryngol 3:174–184

    Article  PubMed  Google Scholar 

  19. Ishida Y, Kobayashi H (1992) Stimulatory effectiveness of amino acids on the olfactory response in an algivorous marine teleost, the rabbitfish Siganus fuscescens Houttuyn. J Fish Biol 41:737–748

    Article  CAS  Google Scholar 

  20. Iwashita A, Sakamoto M, Kojima T, Watanabe Y, Soeda H (1999) Growth effects on the auditory threshold of red sea bream. Nippon Suisan Gakkaishi 65:833–838

    Google Scholar 

  21. Jones GP, Milicich MJ, Emslie MJ, Lunow C (1999) Self-recruitment in a coral reef fish population. Nature 402:802–804

    Article  CAS  Google Scholar 

  22. Kenyon TN (1996) Ontogenetic changes in the auditory sensitivity of damselfishes (Pomacentridae). J Comp Physiol A 179:553–561

    Article  Google Scholar 

  23. Kenyon TN, Ladich F, Yan HY (1998) A comparative study of hearing ability in fishes: the auditory brainstem response approach. J Comp Physiol A 182:307–318

    Article  PubMed  CAS  Google Scholar 

  24. Leis JM (1991) The pelagic stage of reef fishes: the larval biology of coral reef fishes. In: Sale P (ed) The ecology of fishes on coral reefs. Academic, San Diego, pp 183–230

    Google Scholar 

  25. 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 159:165–174

    Article  Google Scholar 

  26. Leis JM, Carson-Ewart BM (1999) In situ swimming and settlement behaviour of larvae of an Indo-Pacific coral-reef fish, the coral trout Plectropomus leopardus (Pisces, Serranidae). Mar Biol 134:51–64

    Article  Google Scholar 

  27. Leis JM, Carson-Ewart BM (2002) In situ settlement behaviour of damselfish (Pomacentridae) larvae. J Fish Biol 61:325–346

    Article  Google Scholar 

  28. Leis JM, Carson-Ewart BM (2003) Orientation of pelagic larvae of coral-reef fishes in the ocean. Mar Ecol Prog Ser 252:239–253

    Article  Google Scholar 

  29. 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 232:259–268

    Article  Google Scholar 

  30. Leis JM, Carson-Ewart BM, Hay AC, Cato DH (2003) Coral-reef sounds enable nocturnal navigation by some reef-fish larvae in some places and at some times. J Fish Biol 63:1–14

    Article  Google Scholar 

  31. Leis JM, Lockett MM (2005) Localization of reef sounds by settlement-stage larvae of coral-reef fishes (Pomacentridae). Bull Mar Sci (in press)

  32. Leis JM, McCormick MI (2002) The biology, behavior, and ecology of the pelagic, larval stage of coral reef fishes. In: Sale P (ed) Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic, San Diego

    Google Scholar 

  33. 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 behavioural capabilities. Mar Freshwater Res 47:401–411

    Article  Google Scholar 

  34. Mann DA, Higgs DM, Tavolga WN, Souza MJ, Popper AN (2001) Ultrasound detection by clupeiform fishes. Acoust Soc Am 109:3048–3054

    Article  CAS  Google Scholar 

  35. McCauley RD, Cato DH (2000) Patterns of fish calling in a nearshore environment in the Great Barrier Reef. Philos Tr Roy Soc Lond B 355:1289–1293

    Article  CAS  Google Scholar 

  36. McCormick MI, Makey L, Dufour V (2002) Comparative study of metamorphosis in tropical reef fishes. Mar Biol 141:841–853

    Article  Google Scholar 

  37. Michel WC, Lubomudrov LM (1995) Specificity and sensitivity of the olfactory organ of the zebrafish, Danio rerio. J Comp Physiol A 177:191–199

    Article  PubMed  CAS  Google Scholar 

  38. Moore A, Waring CP (1996) Electrophysiological and endocrinological evidence that F-series prostaglandins function as priming pheromones in mature male Atlantic salmon (Salmo salar) Parr. J Exp Biol 199:2307–2316

    PubMed  CAS  Google Scholar 

  39. Murphy CA, Stacey NE, Corkum LD (2001) Putative steroidal pheromones in the round goby, Neogobius melanostomus: olfactory and behavioral responses. J Chem Ecol 27:443–470

    Article  PubMed  CAS  Google Scholar 

  40. Myrberg Jr AA, Fuiman LA (2002) The sensory World of coral reef fishes. In: Sale P (ed) Coral reef fishes, pp 123–148

  41. Myrberg Jr AA, Spires JY (1980) Hearing in damselfishes: an analysis of signal detection among closely related species. J Comp Physiol A 140:135–144

    Article  Google Scholar 

  42. Ohman MC, Munday PL, Jones GP, Julian Caley M (1998) Settlement strategies and distribution patterns of coral-reef fishes. J Exp Mar Biol Ecol 225:219–238

    Article  Google Scholar 

  43. Popper AN (1971) The effects of size on auditory capacities of the goldfish. J Audit Res XI:239–247

    Google Scholar 

  44. Roberts CM (1997) Connectivity and management of Caribbean Coral Reefs. Science 278:1454–1457

    Article  PubMed  CAS  Google Scholar 

  45. Rogers PH, Cox M (1988) Underwater sound as a biological stimulus. In: Atema J, Fay RR, Popper AN, Tavolga W (eds) Sensory biology of aquatic animals. Springer, Berlin Heidelberg New York, pp 131–150

    Google Scholar 

  46. Saglio P, Fauconneau B (1985) Free amino acid content in the skin mucus of goldfish, Carassius auratus L.: influence of feeding. Comp Biochem Physiol A 82:67–70

    Article  PubMed  CAS  Google Scholar 

  47. Simpson SD, Meekan MG, McCauley RD, Jeffs A (2004) Attraction of settlement-stage coral reef fishes to reef noise. Mar Ecol Prog Ser 276:263–268

    Article  Google Scholar 

  48. Sorensen PW, Scott AP, Stacey NE, Bowdin L (1995) Sulfated 17,20 beta-dihydroxy-4-pregnen-3-one functions as a potent and specific olfactory stimulant with pheromonal actions in the goldfish. Gen Comp Endocr 100:128–142

    Article  PubMed  CAS  Google Scholar 

  49. Stobutzki IC, Bellwood DR (1997) Sustained swimming abilities of the late pelagic stages of coral reef fishes. Mar Ecol Prog Ser 149:35–41

    Article  Google Scholar 

  50. Stobutzki IC, Bellwood DR (1998) Nocturnal orientation to reefs by late pelagic stage coral reef fishes. Coral Reefs 17:103–110

    Article  Google Scholar 

  51. Swearer SE, Caselle JE, Lea DW, Warner RR (1999) Larval retention and recruitment in an island population of a coral-reef fish. Nature 402:799–802

    Article  CAS  Google Scholar 

  52. Sweatman H (1988) Field evidence that settling coral reef fish larvae detect resident fishes using dissolved chemical cues. J Exp Mar Biol Ecol 124:163–174

    Article  Google Scholar 

  53. Taylor MS, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean Reef Fish. Science 299:107–109

    Article  PubMed  CAS  Google Scholar 

  54. Tolimieri N, Haine O, Jeffs A, McCauley RD, Montgomery JC (2004) Directional orientation of pomacentrid larvae to ambient reef sound. Coral Reefs 23:184–191

    Article  Google Scholar 

  55. 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 207:219–224

    Article  Google Scholar 

  56. Valentincic T, Kralj J, Stenovec M, Koce A, Caprio J (2000) The behavioral detection of binary mixtures of amino acids and their individual components by catfish. J Exp Biol 203:3307–3317

    PubMed  CAS  Google Scholar 

  57. Wysocki LE, Ladich F (2001) The ontogenetic development of auditory sensitivity, vocalization and acoustic communication in the labyrinth fish Trichopsis vittata. J Comp Phys A 187:177–187

    Article  PubMed  CAS  Google Scholar 

  58. Wysocki LE, Ladich F (2003) The representation of conspecific sounds in the auditory brainstem of teleost fishes. J Exp Biol 206:2229–2240

    Article  PubMed  Google Scholar 

  59. Yan HY, Curtsinger WS (2000) The otic gasbladder as an ancillary auditory structure in a mormyrid fish. J Comp Physiol A 186:595–602

    Article  PubMed  CAS  Google Scholar 

  60. Yan HY, Fine ML, Horn NS, Colon WE (2000) Variability in the role of the gasbladder in fish audition. J Comp Physiol A 186:435–445

    Article  PubMed  CAS  Google Scholar 

  61. Zeiske E, Theisen B, Bruecker H (1992) Structure, development, and evolutionary aspects of the peripheral olfactory system. In: Hara TJ (ed) Fish chemoreception. Chapman and Hall, London, pp 13–39

    Google Scholar 

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Acknowledgements

This research was supported by ARC Discovery Grant (DP0345876), DST International Science Linkages Grant (IAP-IST-CG03-00442), and I. Suthers. We thank K. Poling for designing the EOG apparatus, technical advice and draft critiquing, R. Piola for laboratory assistance and draft reading, A. Hay for manuscript revisions and D. Cato for help with the tank design and acoustics. Thanks also to the staff at the Lizard Island Research station for all their assistance.

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Correspondence to K. J. Wright.

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Communicated by M. S. Johnson, Crawley

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Wright, K.J., Higgs, D.M., Belanger, A.J. et al. Auditory and olfactory abilities of pre-settlement larvae and post-settlement juveniles of a coral reef damselfish (Pisces: Pomacentridae). Marine Biology 147, 1425–1434 (2005). https://doi.org/10.1007/s00227-005-0028-z

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Keywords

  • Coral Reef
  • Auditory Brainstem Response
  • Auditory Threshold
  • Sensory Ability
  • Olfactory Ability