Skip to main content
SpringerLink
Log in

Homing ability of adult cardinalfish is affected by elevated carbon dioxide

  • Global change ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The levels of carbon dioxide (CO2) predicted for the oceans by the end of this century have recently been shown to impair olfactory discrimination in larval fishes. However, whether this disruption extends to olfactory-mediated behaviour in adult fishes is unknown. In many fishes, adult survival and reproduction can be critically dependent upon navigation to home sites. We tested the effects that near-future levels of CO2 (550, 700 or 950 ppm) have on the ability of adult five-lined cardinalfish, Cheilodipterus quinquelineatus, to home to their diurnal resting sites after nocturnal feeding. Cardinalfish exposed to elevated CO2 exhibited impaired ability to distinguish between odours of home- versus foreign-site conspecifics in pair-wise choice experiments. A displacement experiment demonstrated that fish from all CO2 treatments displayed a 22–31% reduction in homing success compared with control fish when released at 200 m from home sites. While CO2-exposed cardinalfish released directly back onto home sites exhibited similar site fidelity to control subjects, behaviour at home sites was affected, with CO2-exposed fish exhibiting increased activity levels and venturing further from shelter. This study demonstrates that the potential disruption of chemosensory mechanisms in fishes due to rising CO2 levels in the ocean extend to critical adult behaviours.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • 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. doi:10.3354/meps241151

    Article  Google Scholar 

  • Beukers-Stewart BD, Jones GP (2004) The influence of prey abundance on the feeding ecology of two piscivorous species of coral reef fish. J Exp Mar Biol Ecol 299:155–184. doi:10.1016/j.jembe.2003.08.015

    Article  Google Scholar 

  • Braithwaite VA (1998) Spatial memory, landmark use and orientation in fish. In: Healy S (ed) Spatial representation in animals. Oxford University Press, New York, pp 86–102

    Google Scholar 

  • Broderick AC, Coyne MS, Fuller WJ, Glen F, Godley BJ (2007) Fidelity and over-wintering of sea turtles. Proc R Soc Lond B 274:1533–1539. doi:10.1098/rspb.2007.0211

    Article  Google Scholar 

  • Brown GE, Dreier VM (2002) Predator inspection behaviour and attack cone avoidance in a characin fish: the effects of predator diet and prey experience. Anim Behav 63:1175–1181. doi:10.1006/anbe.2002.3024

    Article  Google Scholar 

  • Chave EH (1978) General ecology of six species of Hawaiian cardinalfishes. Pac Sci 32:245–270

    Google Scholar 

  • Chellappa S, Yamamoto ME, Cacho MSRF, Huntingford FA (1999) Prior residence, body size and the dynamics of territorial disputes between male freshwater angelfish. J Fish Biol 55:1163–1170. doi:10.1111/j.1095-8649.1999.tb02067.x

    Article  Google Scholar 

  • Chrystal PJ, Potter IC, Loneragan NR, Holt CP (1985) Age structure, growth rates, movement patterns and feeding in an estuarine population of the cardinalfish Apogon rueppellii. Mar Biol 85:185–197. doi:10.1007/BF00397437

    Article  Google Scholar 

  • Dalpadado P, Ellertsen B, Melle W, Dommasnes A (2000) Food and feeding conditions of Norwegian spring-spawning herring (Clupea harengus) through its feeding migrations. ICES J Mar Sci 57:843–857. doi:10.1006/jmsc.2000.0573

    Article  Google Scholar 

  • Dawbin WH (1966) The seasonal migratory cycle of humpback whales. In: Norris KS (ed) Whales, dolphins, and porpoises. University of California Press, London, pp 145–170

    Google Scholar 

  • Dittman AH, Quinn TP (1996) Homing in Pacific salmon: mechanisms and ecological basis. J Exp Biol 199:83–91

    PubMed  Google Scholar 

  • 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. doi:10.1111/j.1461-0248.2009.01400.x

    Article  PubMed  Google Scholar 

  • Døving KB, Stabell OB (2003) Trails in open waters: sensory cues in salmon migration. In: Collin SP, Marshal NJ (eds) Sensory processing in aquatic environments. Springer, New York, pp 39–52

    Chapter  Google Scholar 

  • 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. doi:10.1093/chemse/bjj028

    Article  PubMed  Google Scholar 

  • Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414–432. doi:10.1093/icesjms/fsn048

    Article  CAS  Google Scholar 

  • Fukumori K, Okuda N, Yamaoka K, Yanagisawa Y (2010) Remarkable spatial memory in a migratory cardinalfish. Anim Cogn 13:385–389. doi:10.1007/s10071-009-0285-1

    Article  PubMed  Google Scholar 

  • 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. doi:10.1007/s00338-010-0642-1

    Article  Google Scholar 

  • Greenfield DW, Johnson RK (1990) Heterogeneity in habitat choice in cardinalfish community structure. Copeia 1990:1107–1114

    Article  Google Scholar 

  • Hara TJ (1993) The role of olfaction in fish behavior. In: Pitcher TJ (ed) Behaviour of teleost fishes, 2nd edn, Chapman & Hall, London, pp 171–195

  • Hari P, Pumpanen J, Huotari J, Kolari P, Grace J, Vesala T, Ojala A (2008) High-frequency measurements of productivity of planktonic algae using rugged nondispersive infrared carbon dioxide probes. Limnol Oceanogr Meth 6:347–354

    Article  Google Scholar 

  • Heyman WD, Graham RT, Kjerfve B, Johannes RE (2001) Whale sharks Rhincodon typus aggregate to feed on fish spawn in Belize. Mar Ecol Prog Ser 215:275–282

    Article  Google Scholar 

  • Hoegh-Guldberg O et al (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742. doi:10.1126/science.1152509

    Article  PubMed  CAS  Google Scholar 

  • Karnofsky EB, Atema J, Elgin RH (1989) Field observations of social behavior, shelter use, and foraging in the lobster, Homarus americanus. Biol Bull 176:239–246

    Article  Google Scholar 

  • Klimley AP (1993) Highly directional swimming by scalloped hammerhead sharks, Sphyrna lewini, and subsurface irradiance, temperature, bathymetry, and geomagnetic field. Mar Biol 117:1–22. doi:10.1007/BF00346421

    Article  Google Scholar 

  • Lohmann KJ, Putman NF, Lohmann CMF (2008) Geomagnetic imprinting: a unifying hypothesis of long-distance natal homing in salmon and sea turtles. Proc Natl Acad Sci USA 105:19096–19101. doi:10.1073/pnas.0801859105

    Article  PubMed  CAS  Google Scholar 

  • Luschi P, Papi F, Liew HC, Chan EH, Bonadonna F (1996) Long-distance migration and homing after displacement in the green turtle (Chelonia mydas): a satellite tracking study. J Comp Physiol A 178:447–452. doi:10.1007/BF00190175

    Article  Google Scholar 

  • Marnane MJ (2000) Site fidelity and homing behaviour in coral reef cardinalfishes. J Fish Biol 57:1590–1600. doi:10.1006/jfbi.2000.1422

    Article  Google Scholar 

  • Marnane MJ, Bellwood DR (2002) Diet and nocturnal foraging in cardinalfishes (Apogonidae) at One Tree Reef, Great Barrier Reef, Australia. Mar Ecol Prog Ser 231:261–268. doi:10.3354/meps231261

    Article  Google Scholar 

  • Meehl GA et al (2007) Global Climate Projections. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate change 2007: the physical science basis. Cambridge University Press, Cambridge, pp 686–688

    Google Scholar 

  • Meyer CG, Holland KN, Wetherbee BM, Lowe CG (2000) Movement patterns, habitat utilization, home range size and site fidelity of whitesaddle goatfish, Parupeneus prophyreus, in a marine reserve. Envir Biol Fish 59:235–242. doi:10.1023/A:1007664813814

    Article  Google Scholar 

  • Munday PL, Dixson DL, Donelson JM, Jones GP, Pratchett MS, Devitsina GV, Døving KB (2009) Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc Natl Acad Sci USA 106:1848–1852. doi:10.1073/pnas.0809996106

    Article  PubMed  CAS  Google Scholar 

  • Munday PL, Dixson DL, McCormick MI, Meekan M, Ferrari MCO, Chivers DP (2010) Replenishment of fish populations is threatened by ocean acidification. Proc Natl Acad Sci USA 107:12930–12934. doi:10.1073/pnas.1004519107

    Article  PubMed  CAS  Google Scholar 

  • Myrberg AA Jr, Fuiman LA (2002) The sensory world of coral reef fishes. In: Sale PF (ed) Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic, San Diego, pp 123–148

    Google Scholar 

  • Noda M, Gushima K, Kakuda S (1994) Local prey search based on spatial memory and expectation in the planktivorous reef fish, Chromis chrysurus (Pomacentridae). Anim Behav 47:1413–1422. doi:10.1006/anbe.1994.1188

    Article  Google Scholar 

  • O’Gower AK (1995) Speculations on a spatial memory for the Port Jackson shark (Heterodontus portusjacksoni) (Meyer) (Heterodontidae). Mar Freshw Res 46:861–871. doi:10.1071/MF9950861

    Article  Google Scholar 

  • Orr JC et al (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686. doi:10.1038/nature04095

    Article  PubMed  CAS  Google Scholar 

  • Quinn TP (1980) Evidence for celestial and magnetic compass orientation in lake migrating sockeye salmon fry. J Comp Phys A 137:243–248. doi:10.1007/BF00657119

    Article  Google Scholar 

  • Randall JE, Allen GR, Steene RC (1997) Fishes of the Great Barrier Reef and Coral Sea, 2nd edn edn. Crawford House, Bathurst, pp 137–153

    Google Scholar 

  • Raupach MR, Marland G, Ciais P, Le Quéré C, Canadell JG, Klepper G, Field CB (2007) Global and regional drivers of accelerating CO2 emissions. Proc Natl Acad Sci USA 104:10288–10293. doi:10.1073/pnas.0700609104

    Article  PubMed  CAS  Google Scholar 

  • Royal Society (2005) Ocean acidification due to increasing atmospheric carbon dioxide. The Royal Society, London

    Google Scholar 

  • Sale PF (1971) Extremely limited home range in a coral reef fish, Dascyllus aruanus (Pisces; Pomacentridae). Copeia 1971(2):324–327

    Article  Google Scholar 

  • Scholz AT, Horrall RM, Cooper JC, Hasler AD (1976) Imprinting to chemical cues: the basis for home stream selection in salmon. Science 192:1247–1249. doi:10.1126/science.1273590

    Article  PubMed  CAS  Google Scholar 

  • Shapiro DY (1986) Intra-group home ranges in a female-biased group of sex changing fish. Anim Behav 34:865–870. doi:10.1016/S0003-3472(86)80072-0

    Article  Google Scholar 

  • Simpson SD, Munday PL, Wittenrich ML, Manassa R, Dixson DL, Gagliano M, Yan HY (2011) Ocean acidification erodes crucial auditory behaviour in a marine fish. Biol Lett. doi:10.1098/rsbl.2011.0293

  • Tesch F-W (1967) Homing of eels (Anguilla anguilla) in the southern North Sea. Mar Biol 1:4–9. doi:10.1007/BF00346688

    Article  Google Scholar 

  • Turner GF (1994) The fighting tactics of male mouth-brooding cichlids: the effects of size and residency. Anim Behav 47:655–662. doi:10.1006/anbe.1994.1089

    Article  Google Scholar 

  • Willis TJ, Parsons DM, Babcock RC (2001) Evidence for long-term site fidelity in snapper (Pagrus auratus) within a marine reserve. NZ J Mar Freshw Res 35:581–590. doi:10.1080/00288330.2001.9517024

    Article  Google Scholar 

Download references

Acknowledgments

Special thanks to Danielle Dixson and Ingrid Cripps for assistance with field work and the Australian Museum Lizard Island Research Station for providing excellent logistical support and facilities. Funding to P.L.M. from the ARC Centre of Excellence for Coral Reef Studies and to B.M.D. from the Great Barrier Reef Marine Park Authority supported the project. Research was conducted in accordance with JCU ethics approval A1468.

Author information

Authors and Affiliations

  1. ARC Centre of Excellence for Coral Reef Studies, and School of Marine and Tropical Biology, James Cook University, Townsville, QLD, 4811, Australia

    Brynn M. Devine, Philip L. Munday & Geoffrey P. Jones

Authors
  1. Brynn M. Devine
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Philip L. Munday
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Geoffrey P. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Brynn M. Devine.

Additional information

Communicated by Jeff Shima.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Devine, B.M., Munday, P.L. & Jones, G.P. Homing ability of adult cardinalfish is affected by elevated carbon dioxide. Oecologia 168, 269–276 (2012). https://doi.org/10.1007/s00442-011-2081-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-011-2081-2

Keywords

Search

Navigation