Marine Biology

, 165:49 | Cite as

Diel CO2 cycles do not modify juvenile growth, survival and otolith development in two coral reef fish under ocean acidification

  • Michael D. JarroldEmail author
  • Philip L. Munday
Original paper


Recent studies show that daily variation in pCO2 levels can modify the life-history and calcification responses of marine organisms to ocean acidification. The early life stages of coral reef fish exhibit varied growth, survival and otolith development responses to elevated pCO2, yet no studies to date have considered the substantial diel pCO2 cycles that occur in shallow reef habitats. Here, we reared three clutches of juvenile Acanthochromis polyacanthus and Amphiprion percula under control (500 µatm), stable, elevated (1000 µatm) and diel cycling, elevated (1000 ± 300 and 1000 ± 500 µatm) pCO2 for 11 and 6 weeks, respectively. Survival was unaffected by exposure to either elevated stable or diel cycling pCO2 conditions in both species. For A. polyacanthus there was a non-significant trend of decreased standard length and wet weight under stable, elevated pCO2 conditions, whereas values in both the diel cycling treatments were closer to those observed under control conditions. A similar non-significant trend was observed for Am. percula, except that exposure to stable, elevated pCO2 conditions resulted in slightly longer and heavier fish. Finally, otolith size, shape and symmetry in both species were unaffected by exposure to either elevated stable or diel cycling pCO2 conditions. Overall, our results suggest that the growth, survival and otolith development of juvenile coral reef fishes under ocean acidification is unlikely to be affected, in isolation, by diel cycles in pCO2.



We thank Ben Lawes, Simon Wever and Andrew Thompson for their technical support with the aquarium systems at JCU. This project was funded by the Australian Research Council and an ARC Future Fellowship (PLM).

Compliance with ethical standards

Research involving human participants and/or animals

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This research was carried out following approval from the James Cook University animal ethics committee (permit A2210).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

227_2018_3311_MOESM1_ESM.pdf (171 kb)
Supplementary material 1 (PDF 171 kb)


  1. Albright R, Langdon C, Anthony KRN (2013) Dynamics of seawater carbonate chemistry, production, and calcification of a coral reef flat, Central Great Barrier Reef. Biogeosciences 10:6747–6758. CrossRefGoogle Scholar
  2. Alenius B, Munguia P (2012) Effects of pH variability on the intertidal isopod, Paradella dianae. Mar Freshw Behav Physiol 45:245–259. CrossRefGoogle Scholar
  3. Baker DW, Matey V, Huynh KT, Wilson JM, Morgan JD, Brauner CJ (2009) Complete intracellular pH protection during extracellular pH depression is associated with hypercarbia tolerance in white sturgeon, Acipenser transmontanus. Am J Physiol Regul Integr Comp Physiol 296:1868–1880. CrossRefGoogle Scholar
  4. Baumann H, Talmage SC, Gobler CJ (2012) Reduced early life growth and survival in a fish in direct response to increased carbon dioxide. Nat Clim Chang 2:38–41. CrossRefGoogle Scholar
  5. Baumann H, Wallace RB, Tagliaferri T, Gobler CJ (2015) Large Natural pH, CO2 and O2 fluctuations in a temperate tidal salt marsh on diel, seasonal, and interannual time scales. Estuar Coasts 38:220–231. CrossRefGoogle Scholar
  6. Bignami S, Enochs IC, Manzello DP, Sponaugle S, Cowen RK (2013a) Ocean acidification alters the otoliths of a pantropical fish species with implications for sensory function. Proc Natl Acad Sci 110:7366–7370. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bignami S, Sponaugle S, Cowen RK (2013b) Response to ocean acidification in larvae of a large tropical marine fish, Rachycentron canadum. Glob Chang Biol 19:996–1006. CrossRefPubMedGoogle Scholar
  8. Boyd PW, Cornwall CE, Davison A, Doney SC, Fourquez M, Hurd CL, Lima ID, McMinn A (2016) Biological responses to environmental heterogeneity under future ocean conditions. Glob Chang Biol 22:2633–2650. CrossRefPubMedGoogle Scholar
  9. Brauner CJ (2009) Acid-base balance. In: Finn RN, Kapoor BG (eds) Fish larval physiology. Science Publishers, Enfield, pp 185–198Google Scholar
  10. Britton D, Cornwall CE, Revill AT, Hurd CL, Johnson CR (2016) Ocean acidification reverses the positive effects of seawater pH fluctuations on growth and photosynthesis of the habitat-forming kelp, Ecklonia radiata. Sci Rep 6:26036. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365CrossRefPubMedGoogle Scholar
  12. Challener RC, Robbins LL, Mcclintock JB (2016) Variability of the carbonate chemistry in a shallow, seagrass-dominated ecosystem: implications for ocean acidification experiments. Mar Freshw Res 67:163–172. CrossRefGoogle Scholar
  13. Chan WY, Eggins SM (2017) Calcification responses to diurnal variation in seawater carbonate chemistry by the coral Acropora formosa. Coral Reefs. Google Scholar
  14. Checkley DM, Dickson AG, Takahashi M, Radich JA, Eisenkolb N, Asch R (2009) Elevated CO2 enhances otolith growth in young fish. Science 324:1683. CrossRefPubMedGoogle Scholar
  15. Clark HR, Gobler CJ (2016) Do diurnal fluctuations in CO2 and dissolved oxygen concentrations provide a refuge from hypoxia and acidification for early life stage bivalves? Mar Ecol Prog Ser 558:1–14. CrossRefGoogle Scholar
  16. Comeau S, Edmunds PJ, Spindel NB, Carpenter RC (2014) Diel pCO2 oscillations modulate the response of the coral Acropora hyacinthus to ocean acidification. Mar Ecol Prog Ser 501:99–111. CrossRefGoogle Scholar
  17. Cornwall CE, Hepburn CD, McGraw CM, Currie KI, Pilditch CA, Hunter KA, Boyd PW, Hurd CL (2013) Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. Proc R Soc B Biol Sci 280:20132201. CrossRefGoogle Scholar
  18. Davidson MI, Targett TE, Grecay PA (2016) Evaluating the effects of diel-cycling hypoxia and pH on growth and survival of juvenile summer flounder Paralichthys dentatus. Mar Ecol Prog Ser 556:223–235. CrossRefGoogle Scholar
  19. Dickson AG (1990) Standard potential of the reaction: AgCl(s) + 1/2H2(g) = Ag(s) + HCl(aq), and the standard acidity constant of the ion HSO4 in synthetic sea water from 273.15 to 318.15 K. J Chem Thermodyn 22:113–127. CrossRefGoogle Scholar
  20. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res Part A Oceanogr Res Pap 34:1733–1743. CrossRefGoogle Scholar
  21. Dickson AG, Sabine CL, Christian J (2007) Guide to best practices for ocean CO2 measurements. PICES special publication 3. IOCCP report No. 8Google Scholar
  22. 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. CrossRefPubMedGoogle Scholar
  23. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192. CrossRefGoogle Scholar
  24. Doney S, Ruckelshaus M, Duffy E, Barry J, Chan F, English C, Galindo H, Grebmeier J, Hollowed A, Knowlton N, Polovina J, Rabalais N, Sydeman W, Talley L (2012) Climate change impacts on marine ecosystems. Ann Rev Mar Sci 4:11–37. CrossRefPubMedGoogle Scholar
  25. Duarte CM, Hendriks IE, Moore TS, Olsen YS, Steckbauer A, Ramajo L, Carstensen J, Trotter JA, Mcculloch M (2013) Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on seawater pH. Estuar Coasts 36:221–236. CrossRefGoogle Scholar
  26. Dufault AM, Cumbo VR, Fan T, Edmunds PJ (2012) Effects of diurnally oscillating pCO2 on the calcification and survival of coral recruits. Proc R Soc B Biol Sci 279:2951–2958. CrossRefGoogle Scholar
  27. Esbaugh AJ, Heuer R, Grosell M (2012) Impacts of ocean acidification on respiratory gas exchange and acid-base balance in a marine teleost, Opsanus beta. J Comp Physiol B 182:921–934. CrossRefPubMedGoogle Scholar
  28. Franke A, Clemmesen C (2011) Effect of ocean acidification on early life stages of Atlantic herring (Clupea harengus L.). Biogeosciences 8:3697–3707. CrossRefGoogle Scholar
  29. Frieder CA, Nam SH, Martz TR, Levin LA (2012) High temporal and spatial variability of dissolved oxygen and pH in a nearshore California kelp forest. Biogeosciences 9:3917–3930. CrossRefGoogle Scholar
  30. Frieder CA, Gonzalez JP, Bockmon EE, Navarro MO, Levin LA (2014) Can variable pH and low oxygen moderate ocean acidification outcomes for mussel larvae? Glob Chang Biol 20:754–764. CrossRefPubMedGoogle Scholar
  31. Frommel AY, Maneja R, Lowe D, Malzahn AM, Geffen AJ, Folkvord A, Piatkowski U, Reusch TBH, Clemmesen C (2011) Severe tissue damage in Atlantic cod larvae under increasing ocean acidification. Nat Clim Chang 2:42–46. CrossRefGoogle Scholar
  32. Frommel AY, Schubert A, Piatkowski U, Clemmesen C (2013) Egg and early larval stages of Baltic cod, Gadus morhua, are robust to high levels of ocean acidification. Mar Biol 160:1825–1834. CrossRefGoogle Scholar
  33. Gagliano M, Depczynski M, Simpson SD, Moore JAY (2008) Dispersal without errors: symmetrical ears tune into the right frequency for survival. Proc R Soc B Biol Sci 275:527–534. CrossRefGoogle Scholar
  34. Gobler CJ, Clark HR, Griffith AW, Lusty MW (2017) Diurnal fluctuations in acidification and hypoxia reduce growth and survival of larval and juvenile Bay Scallops (Argopecten irradians) and Hard Clams (Mercenaria mercenaria). Front Mar Sci. Google Scholar
  35. Gunderson AR, Armstrong EJ, Stillman JH (2016) Multiple stressors in a changing world: the need for an improved perspective on physiological responses to the dynamic marine environment. Annu Rev Mar Sci 8:1–22. CrossRefGoogle Scholar
  36. Heuer RM, Grosell M (2014) Physiological impacts of elevated carbon dioxide and ocean acidification on fish. Am J Physiol Regul Integr Comp Physiol 307:R1061–R1084. CrossRefPubMedGoogle Scholar
  37. Heuer RM, Welch MJ, Rummer JL, Munday PL, Grosell M (2016) Altered brain ion gradients following compensation for elevated CO2 are linked to behavioural alterations in a coral reef fish. Sci Rep 6:33216. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Hofmann GE, Smith JE, Johnson KS, Send U, Levin LA, Paytan A, Price NN, Peterson B, Takeshita Y, Matson PG, Crook ED, Kroeker KJ, Gambi MC, Rivest EB, Frieder CA, Yu PC, Martz TR (2011) High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS One 6:e28983. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Hurst TP, Fernandez ER, Mathis JT (2013) Effects of ocean acidification on hatch size and larval growth of walleye pollock (Theragra chalcogramma). ICES J Mar Sci 70:812–822CrossRefGoogle Scholar
  40. Ishimatsu A, Hayashi M, Kikkawa T (2008) Fishes in high-CO2, acidified oceans. Mar Ecol Prog Ser 373:295–302. CrossRefGoogle Scholar
  41. Jarrold MD, Humphrey C, McCormick MI, Munday PL (2017) Diel CO2 cycles reduce severity of behavioural abnormalities in coral reef fish under ocean acidification. Sci Rep 7:10153. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kline DI, Teneva L, Hauri C, Schneider K, Miard T, Chai A, Marker M, Dunbar R, Caldeira K, Lazar B, Rivlin T, Mitchell BG, Dove S, Hoegh-Guldberg O (2015) Six month in situ high-resolution carbonate chemistry and temperature study on a coral reef flat reveals asynchronous pH and temperature anomalies. PLoS One 10:e0127648. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Kroeker KJ, Cristina M, Micheli F (2013a) Community dynamics and ecosystem simplification in a high-CO2 ocean. Proc Natl Acad Sci USA 110:12721–12726. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso JP (2013b) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Chang Biol 19:1884–1896. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Lenth RV (2016) Least-squares means: the R Package lsmeans. J Stat Softw 69:1–33. CrossRefGoogle Scholar
  46. Maneja RH, Frommel AY, Geffen AJ, Folkvord A, Piatkowski U, Chang MY, Clemmesen C (2013) Effects of ocean acidification on the calcification of otoliths of larval Atlantic cod Gadus morhua. Mar Ecol Prog Ser 477:251–258. CrossRefGoogle Scholar
  47. Mangan S, Urbina MA, Findlay HS, Wilson RW, Lewis C (2017) Fluctuating seawater pH/pCO2 regimes are more energetically expensive than static pH/pCO2 levels in the mussel Mytilus edulis. Proc R Soc B Biol Sci 284:20171642CrossRefGoogle Scholar
  48. McElhany P, Busch SD (2013) Appropriate pCO2 treatments in ocean acidification experiments. Mar Biol 160:1807–1812. CrossRefGoogle Scholar
  49. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907. CrossRefGoogle Scholar
  50. Meinshausen M, Smith SJ, Calvin K, Daniel JS, Kainuma MLT (2011) The RCP greenhouse gas concentrations and their extensions from 1765 to 2300. Clim Change 109:213–241. CrossRefGoogle Scholar
  51. Melzner F, Gutowska MA, Langenbuch M, Dupont S, Lucassen M, Thorndyke MC, Bleich M, Portner H-O (2009) Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 6:2313–2331CrossRefGoogle Scholar
  52. Moran D, Støttrup JG (2011) The effect of carbon dioxide on growth of juvenile Atlantic cod Gadus morhua L. Aquat Toxicol 102:24–30. CrossRefPubMedGoogle Scholar
  53. Munday PL, Kingsford MJ, O’Callaghan M, Donelson JM (2008) Elevated temperature restricts growth potential of the coral reef fish Acanthochromis polyacanthus. Coral Reefs 27:927–931. CrossRefGoogle Scholar
  54. Munday PL, Donelson JM, Dixson DL, Endo GGK (2009) Effects of ocean acidification on the early life history of a tropical marine fish. Proc R Soc B Biol Sci 276:3275–3283. CrossRefGoogle Scholar
  55. Munday PL, Hernaman V, Dixson DL, Thorrold SR (2011a) Effect of ocean acidification on otolith development in larvae of a tropical marine fish. Biogeosciences 8:1631–1641. CrossRefGoogle Scholar
  56. Munday PL, Gagliano M, Donelson JM, Dixson DL, Thorrold SR (2011b) Ocean acidification does not affect the early life history development of a tropical marine fish. Mar Ecol Prog Ser 423:211–221. CrossRefGoogle Scholar
  57. Nagelkerken I, Connell SD (2015) Global alteration of ocean ecosystem functioning due to increasing human CO2 emissions. Proc Natl Acad Sci 2015:201510856. Google Scholar
  58. Ou M, Hamilton TJ, Eom J, Lyall EM, Gallup J, Jiang A, Lee J, Close DA, Yun S, Brauner CJ (2015) Responses of pink salmon to CO2-induced aquatic acidification. Nat Clim Chang 5:950–955. CrossRefGoogle Scholar
  59. Payan P, De Pontual H, Bœuf G, Mayer-gostan N (2004) Endolymph chemistry and otolith growth in fish. Gen Palaeontol 3:535–547. Google Scholar
  60. Perry DM, Redman DH, Widman JC Jr, Meseck S, King A, Pereira JJ (2015) Effect of ocean acidification on growth and otolith condition of juvenile scup, Stenotomus chrysops. Ecol Evol 5:4187–4196. CrossRefPubMedPubMedCentralGoogle Scholar
  61. Pierrot D, Lewis E, Wallace D (2006) CO2SYS DOS program developed for CO2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory. US Department of Energy, Oak Ridge, TennesseeGoogle Scholar
  62. Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RC (2017) nlme: linear and nonlinear mixed effects models. R package version 3.1-131.
  63. Popper AN, Lu Z (2000) Structure-function relationships in fish otolith organs. Fish Res 46:15–25. CrossRefGoogle Scholar
  64. Przeslawski R, Byrne M, Mellin C (2015) A review and meta-analysis of the effects of multiple abiotic stressors on marine embryos and larvae. Glob Chang Biol 21:2122–2140. CrossRefPubMedGoogle Scholar
  65. Santos IR, Glud RN, Maher D, Erler D, Eyre BD (2011) Diel coral reef acidification driven by porewater advection in permeable carbonate sands, Heron Island, Great Barrier Reef. Geophys Res Lett 38:L03604. CrossRefGoogle Scholar
  66. Shaw EC, McNeil BI, Tilbrook B (2012) Impacts of ocean acidification in naturally variable coral reef flat ecosystems. J Geophys Res 117:C03038. CrossRefGoogle Scholar
  67. Shaw EC, McNeil BI, Tilbrook B, Matear R, Bates ML (2013) Anthropogenic changes to seawater buffer capacity combined with natural reef metabolism induce extreme future coral reef CO2 conditions. Glob Chang Biol 19:1632–1641. CrossRefPubMedGoogle Scholar
  68. Stiasny MH, Mittermayer FH, Sswat M, Voss R, Jutfelt F, Chierici M, Puvanendran V, Mortensen A, Reusch TBH, Clemmesen C (2016) Ocean acidification effects on Atlantic cod larval survival and recruitment to the fished population. PLoS One 11:e0155448. CrossRefPubMedPubMedCentralGoogle Scholar
  69. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  70. Vargas CA, Lagos NA, Lardies MA, Duarte C, Manríquez PH, Aguilera VM, Broitman B, Widdicombe S, Dupont S (2017) Species-specific responses to ocean acidification should account for local adaptation and adaptive plasticity. Nat Ecol Evol. Google Scholar
  71. Wahl M, Saderne V, Sawall Y (2016) How good are we at assessing the impact of ocean acidification in coastal systems? Limitations, omissions and strengths of commonly used experimental approaches with special emphasis on the neglected role of fluctuations. Mar Freshw Res 67:25–36. CrossRefGoogle Scholar
  72. Welch MJ, Watson S-A, Welsh JQ, McCormick MI, Munday PL (2014) Effects of elevated CO2 on fish behaviour undiminished by transgenerational acclimation. Nat Clim Chang 4:1086–1089. CrossRefGoogle Scholar
  73. Wittmann AC, Pörtner H (2013) Sensitivities of extant animal taxa to ocean acidification. Nat Clim Chang 3:995–1001. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.College of Science and EngineeringJames Cook UniversityTownsvilleAustralia
  2. 2.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia

Personalised recommendations