Cues from the reef: olfactory preferences of a symbiotically luminous cardinalfish

Coral Reefs volume 34, pages673–677(2015)Cite this article

Abstract

The symbiotically luminous, reef-dwelling cardinalfish, Siphamia tubifer (Perciformes: Apogonidae), exhibits daily site fidelity, homing behavior, and a preference for the long-spined urchin, Diadema setosum, as its daytime host. The fish acquires its symbiont during larval development and releases large numbers of the bacteria with its feces daily at a host urchin. To examine the role of olfaction in site fidelity and homing by S. tubifer, juvenile and adult fish were tested in a two-channel choice flume for their olfactory preferences. Neither juveniles nor adults showed a preference for seawater conditioned by D. setosum. Juvenile fish, but not adults, preferred seawater conditioned by conspecific fish versus unconditioned seawater. Both juveniles and adults preferred seawater conditioned by their luminous symbiont and also preferred home site water to foreign reef water. These results suggest that S. tubifer uses chemical cues for homing and possibly settlement and symbiont acquisition, but not for host urchin recognition.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2

References

  1. 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 

  2. Brown GE (2003) Learning about danger: chemical alarm cues and local risk assessment in prey fishes. Fish Fish 4:227–234

    Article  CAS  Google Scholar 

  3. Coppock AG, Gardiner NM, Jones GP (2013) Olfactory discrimination in juvenile coral reef fishes: response to conspecifics and corals. J Exp Mar Biol Ecol 443:21–26

    Article  Google Scholar 

  4. Devine BM, Munday PL, Jones GP (2012) Homing ability of adult cardinalfish is affected by elevated carbon dioxide. Oecologia 168:269–276

    Article  PubMed  Google Scholar 

  5. Dixson DL, Munday PL, Jones GP (2010) Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol Lett 13:68–75

    Article  PubMed  Google Scholar 

  6. Dixson DL, Abrego D, Hay M (2014) Chemically mediated behavior of recruiting corals and fishes: a tipping point that may limit reef recovery. Science 345:892–897

    Article  CAS  PubMed  Google Scholar 

  7. Dixson DL, Jones GP, Munday PL, Pratchett MS, Srinivasan M, Planes S, Thorrold SR (2011) Terrestrial chemical cues help coral reef fish larvae locate settlement habitat surrounding islands. Ecol Evol 1:586–595

    Article  PubMed Central  PubMed  Google Scholar 

  8. Dixson DL, Jones GP, Munday PL, Planes S, Pratchett MS, Srinivasan M, Syms C, Thorrold SR (2008) Coral reef fish smell leaves to find island homes. Proc R Soc B Biol Sci 275:2831–2839

    Article  Google Scholar 

  9. Døving KB, Stabell OB, Östlund-Nilsson S, Fisher R (2006) Site fidelity and homing in tropical coral reef cardinalfish: are they using olfactory cues? Chem Senses 31:265–272

    Article  PubMed  Google Scholar 

  10. Dunlap PV, Nakamura M (2011) Functional morphology of the luminescence system of Siphamia versicolor (Perciformes: Apogonidae), a bacterially luminous coral reef fish. J Morphol 272:897–909

    Article  PubMed  Google Scholar 

  11. Dunlap PV, Gould AL, Wittenrich ML, Nakamura M (2012) Symbiosis initiation in the bacterially luminous sea urchin cardinalfish Siphamia versicolor. J Fish Biol 81:1340–1356

    Article  CAS  PubMed  Google Scholar 

  12. Fukumori K, Okuda N, Yamaoka K, Yanagisawa Y (2010) Remarkable spatial memory in a migratory cardinalfish. Anim Cogn 13:385–389

    Article  PubMed  Google Scholar 

  13. Gardiner NM, Jones GP (2010) Synergistic effects of habitat preference and gregarious behaviour on habitat use in coral reef cardinalfish. Coral Reefs 29:845–856

    Article  Google Scholar 

  14. Gerlach G, Atema J (2012) The use of chemical cues in habitat recognition and settlement. In: Brönmark C, Hansson L-A (eds) Chemical ecology in aquatic systems. Oxford University Press, New York, pp 75–79

    Google Scholar 

  15. Gerlach G, Atema J, Kingsford MJ, Black KP, Miller-Sims V (2007) Smelling home can prevent dispersal of reef fish larvae. Proc Natl Acad Sci 3:858–863

    Article  Google Scholar 

  16. Gould AL, Harii S, Dunlap PV (2014) Host preference, site fidelity, and homing behavior of the symbiotically luminous cardinalfish, Siphamia tubifer (Perciformes: Apogonidae). Mar Biol 161:2897–2907

    Article  Google Scholar 

  17. Kolm N, Hoffman EA, Olsson J, Berglund A, Jones AG (2005) Group stability and homing behavior but no kin group structures in a coral reef fish. Behav Ecol 16:521–527

    Article  Google Scholar 

  18. 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 63:724–737

    Article  Google Scholar 

  19. Marnane MJ (2000) Site fidelity and homing behaviour in coral reef cardinalfishes. J Fish Biol 57:1590–1600

    Article  Google Scholar 

  20. Munday PL, Pratchett MS, Dixson DL, Donelson JM, Endo GG, Reynolds AD, Knuckey R (2013) Elevated CO2 affects the behavior of an ecologically and economically important coral reef fish. Mar Biol 160:2137–2144

    Article  CAS  Google Scholar 

  21. R Development Core Team (2012) R: a language and environment for statistical computing, vol R 2.15.1. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  22. Radford CA, Jeffs AG, Tindle CT, Montgomery JC (2008) Resonating sea urchin skeletons create coastal choruses. Mar Ecol Prog Ser 362:37–43

    Article  Google Scholar 

  23. Radford CA, Stanley JA, Tindle CT, Montgomery JC, Jeffs AG (2010) Localised coastal habitats have distinct underwater sound signatures. Mar Ecol Prog Ser 401:21–29

    Article  Google Scholar 

  24. 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 

  25. Simpson SD, Meekan MG, Montgomery JC, McCauley RD, Jeffs AG (2005) Homeward sound. Science 308:221

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank J. Dobkowski and M. Grundler (University of Michigan) for technical assistance. Support was provided by the PADI Foundation.

Author information

Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Michigan, 830 North University Avenue, Ann Arbor, MI, 48109, USA

    Alison L. Gould & Paul V. Dunlap

  2. Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus, Motobu, Okinawa, 905-0227, Japan

    Saki Harii

Authors
  1. Alison L. Gould
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saki Harii
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul V. Dunlap
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alison L. Gould.

Additional information

Communicated by Biology Editor Dr. Andrew Hoey

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gould, A.L., Harii, S. & Dunlap, P.V. Cues from the reef: olfactory preferences of a symbiotically luminous cardinalfish. Coral Reefs 34, 673–677 (2015). https://doi.org/10.1007/s00338-015-1278-y

Download citation

Keywords

  • Siphamia tubifer
  • Apogonidae
  • Olfaction
  • Homing
  • Bioluminescence
  • Symbiosis