Skip to main content

Impact of ocean acidification in the metabolism and swimming behavior of the dolphinfish (Coryphaena hippurus) early larvae

Abstract

Since the industrial revolution, [CO2]atm has increased from 280 μatm to levels now exceeding 380 μatm and is expected to rise to 730–1,020 μatm by the end of this century. The consequent changes in the ocean’s chemistry (e.g., lower pH and availability of the carbonate ions) are expected to pose particular problems for marine organisms, especially in the more vulnerable early life stages. The aim of this study was to investigate how the future predictions of ocean acidification may compromise the metabolism and swimming capabilities of the recently hatched larvae of the tropical dolphinfish (Coryphaena hippurus). Here, we show that the future environmental hypercapnia (ΔpH 0.5; 0.16 % CO2, ~1,600 μatm) significantly (p < 0.05) reduced oxygen consumption rate up to 17 %. Moreover, the swimming duration and orientation frequency also decreased with increasing pCO2 (50 and 62.5 %, respectively). We argue that these hypercapnia-driven metabolic and locomotory challenges may potentially influence recruitment, dispersal success, and the population dynamics of this circumtropical oceanic top predator.

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

Fig. 1

References

  1. Anderson JT (1988) A review of size dependent survival during pre-recruit stages of fishes in relation to recruitment. J Northw Atl Fish Sci 8:55–56

    Google Scholar 

  2. Baumann H, Talmage SC, Gobler CJ (2012) Reduced early life growth and survival in a fish in direct response to increased carbon dioxide. Nature Clim Change 2(1):38–41. doi:10.1038/nclimate1291

    CAS  Article  Google Scholar 

  3. Beardsley GL (1967) Age, growth and reproduction of the dolphin, Coryphaena hippurus, in the straits of Florida. Copeia

  4. Benetti DD, Alarcon JF, Stevens OM, O’Hanlon B, Rivera JA, Banner-Stevens G, Rotman FJ (2003) Advances in hatchery and growout technology of marine finfish candidate species for offshore aquaculture in the Caribbean. In: Proceedings of the fifty-fourth annual gulf and Caribbean Fisheries Institute

  5. Bignami SGT (2013) Effects of ocean acidification on the early life history of two pelagic tropical fish species, Cobia (Rachycentron canadum) and Mahi-mahi (Coryphaena hippurus). Electronic theses and dissertations open access dissertations, paper 981, University of Miami, Miami, Florida

  6. Byrne M (2011) Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerability and potential for persistence in a changing ocean. Oceanogr Mar Biol 49:1–42

    Google Scholar 

  7. Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110 (C9). doi:10.1029/2004jc002671

  8. Castro JJ, Santiago JA, Hernández-García V, Pla C (1999) Growth and reproduction of the dolphinfish (Coryphaena equiselis and Coryphaena hippurus) in the Canary Islands, Central-East Atlantic (preliminary results). Sci Mar 63(3–4):317–325

    Google Scholar 

  9. Dixson DL, Munday PL, Jones GP (2010) Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol Lett 13(1):68–75. doi:10.1111/j.1461-0248.2009.01400.x

    Article  Google Scholar 

  10. Domenici P, Allan B, McCormick MI, Munday PL (2012) Elevated carbon dioxide affects behavioural lateralization in a coral reef fish. Biol Lett 8(1):78–81. doi:10.1098/rsbl.2011.0591

    CAS  Article  Google Scholar 

  11. Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. Ices Mar Res 65(3):414–432. doi:10.1093/icesjms/fsn048

    CAS  Article  Google Scholar 

  12. Ferrari MCO, Manassa RP, Dixson DL, Munday PL, McCormick MI, Meekan MG, Sih A, Chivers DP (2012a) Effects of ocean acidification on learning in coral reef fishes. Plos ONE 7(2). doi:10.1371/journal.pone.0031478

  13. Franke A, Clemmesen C (2011) Effect of ocean acidification on early life stages of Atlantic herring (Clupea harengus L.). Biogeosci Discuss 8(12):3697–3707. doi:10.5194/bg-8-3697-2011

    CAS  Article  Google Scholar 

  14. Frommel AY, Maneja R, Lowe D, Malzahn AM, Geffen AJ, Folkvord A, Piatkowski U, Reusch TBH, Clemmesen C (2012) Severe tissue damage in Atlantic cod larvae under increasing ocean acidification. Nature Clim Change 2(1):42–46. doi:10.1038/climate1324

    CAS  Article  Google Scholar 

  15. Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanisms and process in physiological evolution. Oxford University Press, Oxford

    Google Scholar 

  16. Hurst TP, Cooper DW, Scheingross JS, Seale EM, Laurel BJ, Spencer ML (2009) Effects of ontogeny, temperature, and light on vertical movements of larval Pacific cod (Gadus macrocephalus). Fish Oceanogr 18(5):301–311. doi:10.1111/j.1365-2419.2009.00512.x

    Article  Google Scholar 

  17. Ishimatsu A, Hayashi M, Kikkawa T (2008) Fishes in high-CO2, acidified oceans. Mar Ecol Prog Ser 373:295–302. doi:10.3354/meps07823

    CAS  Article  Google Scholar 

  18. Leis JM (2006) Are larvae of demersal fishes plankton or nekton? Adv Mar Biol 51:57–141

    Article  Google Scholar 

  19. Lewis E, Wallace DWR (1998) CO2SYS-Program developed for the CO2 system calculations. Carbon Dioxide Inf Anal Center, Report ORNL/CDIAC-105

  20. Maneja RH, Frommel AY, Browman HI, Clemmesen C, Geffen AJ, Folkvord A, Piatkowski U, Durif CMF, Bjelland R, Skiftesvik AB (2013) The swimming kinematics of larval Atlantic cod, Gadus morhua L., are resilient to elevated seawater pCO2. Mar Biol 160:1963–1972

    CAS  Article  Google Scholar 

  21. Martin P, Bateson P (1993) Measuring behavior: an introductory guide. Cambridge University Press, Cambridge

    Book  Google Scholar 

  22. Meehl GA, Stocker TF, Collins WD, Friedlingstein P, Gaye AT, Gregory JM, Kitoh A, Knutti R, Murphy JM, Noda.A, Raper SCB, Watterson IG, Weaver AJ, Zhao ZC (2007) Climate change 2007: the physical science basis. Contribution of Working Group I to the fourth assessment report of the intergovernmental panel on climate change. Climate change 2007: the physical science basis. Cambridge University Press, Cambridge, UK

  23. Munday PL, Dixson DL, Donelson JM, Jones GP, Pratchett MS, Devitsina GV, Doving KB (2009) Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. PNAS 106(6):1848–1852

    CAS  Article  Google Scholar 

  24. Munday PL, Dixson DL, McCormick MI, Meekan M, Ferrari MCO, Chivers DP (2010) Replenishment of fish populations is threatened by ocean acidification. PNAS 107(29):12930–12934. doi:10.1073/pnas.1004519107

    CAS  Article  Google Scholar 

  25. Oxenford HA (1999) Biology of the dolphinfish (Coryphaena hippurus) in the western central Atlantic: a review. Sci Mar 63 (3 − 4):277 − 301

    Google Scholar 

  26. Perez FF, Rios AF, Roson G (1999) Sea surface carbon dioxide off the Iberian Peninsula (North Eastern Atlantic Ocean). J Marine Syst 19(1–3):27–46. doi:10.1016/s0924-7963(98)00022-0

    Article  Google Scholar 

  27. Perry SF, Gilmour KM (2006) Acid-base balance and CO2 excretion in fish: unanswered questions and emerging models. Respir Physiol Neurobiol 154(1–2):199–215. doi:10.1016/j.resp.2006.04.010

    CAS  Article  Google Scholar 

  28. Pimentel MS, Trubenbach K, Faleiro F, Boavida-Portugal J, Repolho T, Rosa R (2012) Impact of ocean warming on the early ontogeny of cephalopods: a metabolic approach. Mar Biol 159(9):2051–2059. doi:10.1007/s00227-012-1991-9

    Article  Google Scholar 

  29. Portner HO, Langenbuch M, Reipschlager A (2004) Biological impact of elevated ocean CO2 concentrations: Lessons from animal physiology and earth history. J Ocean 60(4):705–718. doi:10.1007/s10872-004-5763-0

    Article  Google Scholar 

  30. Portner HO, Langenbuch M, Michaelidis B (2005) Synergistic effects of temperature extremes, hypoxia, and increases in CO2 on marine animals: From Earth history to global change. J Geophys Res Oceans 110 (C9). doi:10.1029/2004jc002561

  31. Rodrigues N, Correia J, Pinho R, Graca J, Rodrigues F, Hirofumi M (2013) Notes on the husbandry and long-term transportation of bull ray (Pteromylaeus bovinus) and dolphinfish (Coryphaena hippurus and Coryphaena equiselis). Zoo Biol 32(2):222–229. doi:10.1002/zoo.21048

    Article  Google Scholar 

  32. Rosa R, Pimentel MS, Boavida-Portugal J, Teixeira T, Trubenbach K, Diniz M (2012) Ocean warming enhances malformations, premature hatching,metabolic suppression and oxidative stress in the early life stages of a keystone squid. Plos ONE 7 (6). doi:10.1371/journal.pone.0038282

  33. Rosa R, Trübenbach K, Repolho T, Pimentel M, Faleiro F, Boavida-Portugal J, Baptista M, Lopes VM, Dionísio G, Leal M, Calado R, Pörtner HO (2013) Lower hypoxia thresholds of cuttlefish early life stages living in a warm acidified ocean. Proc R Soc Lond B. doi:10.1098/rspb.2013.1695

    Google Scholar 

  34. Rosa R, Trübenbach K, Pimentel MS, Boavida-Portugal J, Faleiro F, Baptista M, Dionísio G, Calado R, Pörtner HO, Repolho T (in press) Differential impacts of ocean acidification and warming on winter and summer progeny of a coastal squid (Loligo vulgaris). J Exp Biol

  35. Sarazin G, Michard G, Prevot F (1999) A rapid and accurate spectroscopic method for alkalinity measurements in seawater samples. Water Res 33:290–294

    CAS  Article  Google Scholar 

  36. 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 7(6):917–920. doi:10.1098/rsbl2011.0293

    CAS  Article  Google Scholar 

  37. Stanley RRE (2009) A biophysical study of connectivity in the early life history of coastal Newfoundland fishes. Memorial University of Newfoundland, St. John’s

  38. Storey KB, Storey JM (2004) Oxygen limitation and metabolic rate depression. In: Storey KB (ed) Functional metabolism. Regulation and adaptation.Wiley, Hobocken, NJ, pp 415–442

    Chapter  Google Scholar 

  39. Talmage SC, Gobler CJ (2010) Effects of past, present, and future ocean carbon dioxide concentrations on the growth and survival of larval shellfish. PNAS 107(40):17246–17251. doi:10.1073/pnas.0913804107

    CAS  Article  Google Scholar 

  40. Tojeira I, Faria AM, Henriques S, Faria C, Gonçalves EJ (2012) Early development and larval behaviour of two clingfishes, Lepadogaster purpurea and Lepadogaster lepadogaster (Pisces: Gobiesocidae). Environ Biol Fish 93:449–459

    Article  Google Scholar 

  41. Vikebø F, Jørgensen C, Kristiansen T, Fiksen Ø (2007) Drift, growth and survival of larval Northeast Arctic cod with simple rules of behaviour. Mar Ecol Prog 347:207–219

    Article  Google Scholar 

Download references

Acknowledgments

The authors would like to thank University of Miami Experimental Hatchery (UMEH) of the Rosenstiel School of Marine and Atmospheric Science (RSMAS), Daniel Benetti, Carlos Reis, José Graça, and to TUNIPEX, S.A. for supplying fish eggs. The Portuguese Foundation for Science and Technology (FCT) supported this study through a doctoral Grant SFRH/BD/81928/2011 to M.S.P. and through the projects PTDC/BIA-BEC/103266/2008 and PTDC/MAR/0908066/2008 to R.R.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Marta Pimentel.

Additional information

Communicated by M. A. Peck.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Pimentel, M., Pegado, M., Repolho, T. et al. Impact of ocean acidification in the metabolism and swimming behavior of the dolphinfish (Coryphaena hippurus) early larvae. Mar Biol 161, 725–729 (2014). https://doi.org/10.1007/s00227-013-2365-7

Download citation

Keywords

  • Ocean Acidification
  • Early Life Stage
  • Swimming Behavior
  • pCO2 Condition
  • Hypercapnic Condition