Advertisement

Physiological implications of ocean acidification for marine fish: emerging patterns and new insights

Abstract

Ocean acidification (OA) is an impending environmental stress facing all marine life, and as such has been a topic of intense research interest in recent years. Numerous detrimental effects have been documented in marine fish, ranging from reduced mortality to neurosensory impairment, and the prevailing opinions state that these effects are largely the downstream consequences of altered blood carbon dioxide chemistry caused by respiratory acid–base disturbances. While the respiratory acid–base disturbances are consistent responses to OA across tested fish species, it is becoming increasingly clear that there is wide variability in the degree of downstream impairments between species. This can also be extended to intraspecies variability, whereby some individuals have tolerant physiological traits, while others succumb to the effects of OA. This review will synthesize relevant literature on marine fish to highlight consistent trends of impairment, as well as observed interspecies variability in the responses to OA, and the potential routes of physiological acclimation. In all cases, whole animal responses are linked to demonstrated or proposed physiological impairments. Major topics of focus include: (1) respiratory acid–base disturbances; (2) early life survival and growth; (3) the implications for metabolic performance, activity, and reproduction; and (4) emerging physiological theories pertaining to neurosensory impairment and the role of GABAA receptors. Particular emphasis is placed on the importance of understanding the underlying physiological traits that confer inter- and intraspecies tolerance, as the abundance of these traits will decide the long-term outlook of marine fish.

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

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Alderman SL, Harter TS, Wilson JM, Supuran CT, Farrell AP, Brauner CJ (2016) Evidence for a plasma-accessible carbonic anhydrase in the lumen of salmon heart that may enhance oxygen delivery to the myocardium. J Exp Biol 219(Pt 5):719–724

  2. Allmon EB, Esbaugh AJ (2017) Carbon dioxide induced plasticity of branchial acid–base pathways in an estuarine teleost. Sci Rep 7:45680

  3. Altieri AH, Gedan KB (2015) Climate change and dead zones. Glob Chang Biol 21(4):1395–1406

  4. 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(6):R1868–R1880

  5. 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 Change 2:38–41

  6. Bell G (2013) Evolutionary rescue and the limits of adaptation. Philos Trans R Soc Lond B Biol Sci 368(1610):20120080

  7. Berenbrink M, Koldkjaer P, Kepp O, Cossins AR (2005) Evolution of oxygen secretion in fishes and the emergence of a complex physiological system. Science 307(5716):1752–1757

  8. 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 USA 110(18):7366–7370

  9. 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(4):996–1006

  10. Bignami S, Sponaugle S, Cowen RK (2014) Effects of ocean acidification on the larvae of a high-value pelagic fisheries species, mahi–mahi Coryphaena hippurus. Aquat Biol 21(3):249–260

  11. Bromhead D, Scholey V, Nicol S, Margulies D, Wexler J, Stein M, Hoyle S, Lennert-Cody C, Williamson J, Havenhand J, Ilyina T, Lehodey P (2015) The potential impact of ocean acidification upon eggs and larvae of yellowfin tuna (Thunnus albacares). Deep sea research Part II: topical studies. Oceanography 113:268–279

  12. Casper BM, Mann DA (2007) Dipole hearing measurements in elasmobranch fishes. J Exp Biol 210(Pt 1):75–81

  13. Castro JM, Amorim MC, Oliveira AP, Goncalves EJ, Munday PL, Simpson SD, Faria AM (2017) Painted goby larvae under high-CO2 fail to recognize reef sounds. PLOS One 12(1):e0170838

  14. Catches JS, Burns JM, Edwards SL, Claiborne JB (2006) Na+/H+ antiporter, V-H+-ATPase and Na+/K+-ATPase immunolocalization in a marine teleost (Myoxocephalus octodecemspinosus). J Exp Biol 209(Pt 17):3440–3447

  15. Chambers RC, Candelmo AC, Habeck EA, Poach ME, Wieczorek D, Cooper KR, Greenfield CE, Phelan BA (2014) Effects of elevated CO2 in the early life stages of summer flounder, Paralichthys dentatus, and potential consequences of ocean acidification. Biogeosciences 11(6):1613–1626

  16. Checkley DM Jr, Dickson AG, Takahashi M, Radich JA, Eisenkolb N, Asch R (2009) Elevated CO2 enhances otolith growth in young fish. Science 324(5935):1683

  17. Chung WS, Marshall NJ, Watson SA, Munday PL, Nilsson GE (2014) Ocean acidification slows retinal function in a damselfish through interference with GABAA receptors. J Exp Biol 217(Pt 3):323–326

  18. Claiborne JB, Choe KP, Morrison-Shetlar AI, Weakley JC, Havird J, Freiji A, Evans DH, Edwards SL (2008) Molecular detection and immunological localization of gill Na+/H+ exchanger in the dogfish (Squalus acanthias). Am J Physiol Regul Integr Comp Physiol 294(3):R1092–R1102

  19. Claireaux G, Theron M, Prineau M, Dussauze M, Merlin FX, Le Floch S (2013) Effects of oil exposure and dispersant use upon environmental adaptation performance and fitness in the European sea bass, Dicentrarchus labrax. Aquat Toxicol 130–131:160–170

  20. Couturier CS, Stecyk JA, Rummer JL, Munday PL, Nilsson GE (2013) Species-specific effects of near-future CO(2) on the respiratory performance of two tropical prey fish and their predator. Comp Biochem Physiol A Mol Integr Physiol 166(3):482–489

  21. Cripps IL, Munday PL, McCormick MI (2011) Ocean acidification affects prey detection by a predatory reef fish. PLoS One 6(7):e22736

  22. Davis BE, Miller NA, Flynn EE, Todgham AE (2016) Juvenile Antarctic rockcod Trematomus bernacchii are physiologically robust to CO2-acidified seawater. J Exp Biol 219(8):1203–1213

  23. DePasquale E, Baumann H, Gobler CJ (2015) Vulnerability of early life stage Northwest Atlantic forage fish to ocean acidification and low oxygen. Mar Ecol Prog Ser 523:145–156

  24. Di Santo V (2016) Intraspecific variation in physiological performance of a benthic elasmobranch challenged by ocean acidification and warming. J Exp Biol 219(11):1725

  25. 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

  26. Dixson DL, Jennings AR, Atema J, Munday PL (2015) Odor tracking in sharks is reduced under future ocean acidification conditions. Glob Chang Biol 21(4):1454–1462

  27. Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Ann Rev Mar Sci 1:169–192

  28. Edwards SL, Wall BP, Morrison-Shetlar A, Sligh S, Weakley JC, Claiborne JB (2005) The effect of environmental hypercapnia and salinity on the expression of NHE-like isoforms in the gills of a euryhaline fish (Fundulus heteroclitus). J Exp Zool Part A Comp Exp Biol 303 A(6):464–475

  29. Ern R, Esbaugh AJ (2016) Hyperventilation and blood acid–base balance in hypercapnia exposed red drum (Sciaenops ocellatus). J Comp Physiol B 186(4):447–460

  30. 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(7):921–934

  31. Esbaugh AJ, Ern R, Nordi WM, Johnson AS (2016) Respiratory plasticity is insufficient to alleviate blood acid–base disturbances after acclimation to ocean acidification in the estuarine red drum, Sciaenops ocellatus. J Comp Physiol B 186(1):97–109

  32. Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid–base regulation, and excretion of nitrogenous waste. Physiol Rev 85(1):97–177

  33. Ferrari MC, Manassa RP, Dixson DL, Munday PL, McCormick MI, Meekan MG, Sih A, Chivers DP (2012) Effects of ocean acidification on learning in coral reef fishes. PLoS One 7(2):e31478

  34. Franke A, Clemmesen C (2011) Effect of ocean acidification on early life stages of Atlantic herring (Clupea harengus L.). Biogeosciences 8(12):3697–3707

  35. Frommel A, 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. Nat Clim Change 2:42–46

  36. 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(8):1825–1834

  37. Frommel AY, Maneja R, Lowe D, Pascoe CK, Geffen AJ, Folkvord A, Piatkowski U, Clemmesen C (2014) Organ damage in Atlantic herring larvae as a result of ocean acidification. Ecol Appl Publ Ecol Soc Am 24(5):1131–1143

  38. Frommel AY, Margulies D, Wexler JB, Stein MS, Scholey VP, Williamson JE, Bromhead D, Nicol S, Havenhand J (2016) Ocean acidification has lethal and sub-lethal effects on larval development of yellowfin tuna, Thunnus albacares. J Exp Mar Biol Ecol 482:18–24

  39. Gilmour KM, Perry SF (2007) Branchial chemoreceptor regulation of cardiorespiratory function. In: Hara T, Zielinski B (eds) Fish physiology vol 25: sensory systems neuroscience. Academic Press, New York, pp 97–151

  40. Godbold JA, Calosi P (2013) Ocean acidification and climate change: advances in ecology and evolution. Philos Trans R Soc Lond B Biol Sci 368(1627):20120448

  41. Gonzalez A, Ronce O, Ferriere R, Hochberg ME (2013) Evolutionary rescue: an emerging focus at the intersection between ecology and evolution. Philos Trans R Soc Lond B Biol Sci 368(1610):20120404

  42. Goulet CT, Thompson MB, Chapple DG (2017) Repeatability and correlation of physiological traits: do ectotherms have a “thermal type”? Ecol Evol 7(2):710–719

  43. Grans A, Jutfelt F, Sandblom E, Jonsson E, Wiklander K, Seth H, Olsson C, Dupont S, Ortega-Martinez O, Einarsdottir I, Bjornsson BT, Sundell K, Axelsson M (2014) Aerobic scope fails to explain the detrimental effects on growth resulting from warming and elevated CO2 in Atlantic halibut. J Exp Biol 217(Pt 5):711–717

  44. Green L, Jutfelt F (2014) Elevated carbon dioxide alters the plasma composition and behaviour of a shark. Biol Lett 10(9):20140538

  45. Hamilton TJ, Holcombe A, Tresguerres M (2014) CO2 induced ocean acidification increases anxiety in Rockfish via alteration of GABA-A receptor functioning. Proc R Soc B Biol Sci 281(1775):20132509

  46. Hamilton SL, Logan CA, Fennie HW, Sogard SM, Barry JP, Makukhov AD, Tobosa LR, Boyer K, Lovera CF, Bernardi G (2017) Species-specific responses of juvenile rockfish to elevated pCO2: from behavior to genomics. PLoS One 12(1):e0169670

  47. Harvey BP, Gwynn-Jones D, Moore PJ (2013) Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecol Evol 3(4):1016–1030

  48. Heuer RM, Grosell M (2014) Physiological impacts of elevated carbon dioxide and ocean acidification on fish. Am J Physiol Regul Integr Comp Physiol 307(9):R1061–R1084

  49. Heuer RM, Grosell M (2016) Elevated CO2 increases energetic cost and ion movement in the marine fish intestine. Sci Rep 6:34480

  50. Heuer RM, Esbaugh AJ, Grosell M (2012) Ocean acidification leads to counterproductive intestinal base loss in the gulf toadfish (Opsanus beta). Physiol Biochem Zool 85(5):450–459

  51. 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

  52. Hofmann GE, Todgham AE (2010) Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annu Rev Physiol 72:127–145

  53. Honisch B, Ridgwell A, Schmidt DN, Thomas E, Gibbs SJ, Sluijs A, Zeebe R, Kump L, Martindale RC, Greene SE, Kiessling W, Ries J, Zachos JC, Royer DL, Barker S, Marchitto TM Jr, Moyer R, Pelejero C, Ziveri P, Foster GL, Williams B (2012) The geological record of ocean acidification. Science 335(6072):1058–1063

  54. Huijbers CM, Nagelkerken I, Lossbroek PA, Schulten IE, Siegenthaler A, Holderied MW, Simpson SD (2012) A test of the senses: fish select novel habitats by responding to multiple cues. Ecology 93(1):46–55

  55. IPCC (2014) Climate change 2014: synthesis report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. In: Pachauri RK, Meyer LA (eds) IPCC, Geneva, p 151

  56. Kahle KT, Deeb TZ, Puskarjov M, Silayeva L, Liang B, Kaila K, Moss SJ (2013) Modulation of neuronal activity by phosphorylation of the K–Cl cotransporter KCC2. Trends Neurosci 36(12):726–737

  57. Kaila K, Ruusuvuori E, Seja P, Voipio J, Puskarjov M (2014) GABA actions and ionic plasticity in epilepsy. Curr Opin Neurobiol 26:34–41

  58. Kelly MW, Hofmann GE (2013) Adaptation and the physiology of ocean acidification. Funct Ecol 27(4):980–990

  59. Khirug S, Yamada J, Afzalov R, Voipio J, Khiroug L, Kaila K (2008) GABAergic depolarization of the axon initial segment in cortical principal neurons is caused by the Na-K-2Cl cotransporter NKCC1. J Neurosci 28(18):4635–4639

  60. Killen SS, Adriaenssens B, Marras S, Claireaux G, Cooke SJ (2016) Context dependency of trait repeatability and its relevance for management and conservation of fish populations. Conserv Physiol 4(1):cow007

  61. Kreiss CM, Michael K, Bock C, Lucassen M, Portner HO (2015) Impact of long-term moderate hypercapnia and elevated temperature on the energy budget of isolated gills of Atlantic cod (Gadus morhua). Comp Biochem Physiol A Mol Integr Physiol 182:102–112

  62. Kunz KL, Frickenhaus S, Hardenberg S, Johansen T, Leo E, Portner HO, Schmidt M, Windisch HS, Knust R, Mark FC (2016) New encounters in Arctic waters: a comparison of metabolism and performance of polar cod (Boreogadus saida) and Atlantic cod (Gadus morhua) under ocean acidification and warming. Polar Biol 39(6):1137–1153

  63. Lai F, Jutfelt F, Nilsson GE (2015) Altered neurotransmitter function in CO2-exposed stickleback (Gasterosteus aculeatus): a temperate model species for ocean acidification research. Conserv Physiol 3(1):cov018

  64. Leduc AO, Munday PL, Brown GE, Ferrari MC (2013) Effects of acidification on olfactory-mediated behaviour in freshwater and marine ecosystems: a synthesis. Philos Trans R Soc Lond B Biol Sci 368(1627):20120447

  65. Lefevre S (2016) Are global warming and ocean acidification conspiring against marine ectotherms? A meta-analysis of the respiratory effects of elevated temperature, high CO2 and their interaction. Conserv Physiol 4(1):cow009

  66. Liu ST, Tsung L, Horng JL, Lin LY (2013) Proton-facilitated ammonia excretion by ionocytes of medaka (Oryzias latipes) acclimated to seawater. Am J Physiol Regul Integr Comp Physiol 305(3):R242–R251

  67. Lonthair J, Ern R, Esbaugh AJ (2017) Early life stages of an estuarine-dependent fish are tolerant of ocean acidification. ICES J Mar Sci

  68. Lopes AF, Morais P, Pimentel M, Rosa R, Munday PL, Goncalves EJ, Faria AM (2016) Behavioural lateralization and shoaling cohesion of fish larvae altered under ocean acidification. Mar Biol 163 (12)

  69. Marshall WS, Grosell M (2006) Ion Transport, osmoregulation, and acid–base balance. In: Evans DH, Claiborne JB (eds) The physiology of fishes, 3rd edn. Taylor and Francis Group, New York, pp 177–230

  70. Medina I, Friedel P, Rivera C, Kahle KT, Kourdougli N, Uvarov P, Pellegrino C (2014) Current view on the functional regulation of the neuronal K(+)–Cl(-) cotransporter KCC2. Front Cell Neurosci 8:27

  71. Melzner F, Gobel S, Langenbuch M, Gutowska MA, Portner HO, Lucassen M (2009) Swimming performance in Atlantic Cod (Gadus morhua) following long-term (4–12 months) acclimation to elevated seawater PCO2. Aquat Tox 92(1):30–37

  72. Michael K, Kreiss CM, Hu MY, Koschnick N, Bickmeyer U, Dupont S, Portner HO, Lucassen M (2016) Adjustments of molecular key components of branchial ion and pH regulation in Atlantic cod (Gadus morhua) in response to ocean acidification and warming. Comp Biochem Physiol B Biochem Mol Biol 193:33–46

  73. Miller GM, Watson S, Donelson JM, McCormick MI, Munday PL (2012) Parental environment mediates impacts of increased carbon dioxide on a coral reef fish. Nat Clim Change 2:858–861

  74. Miller GM, Watson SA, McCormick MI, Munday PL (2013) Increased CO2 stimulates reproduction in a coral reef fish. Glob Chang Biol 19(10):3037–3045

  75. Mu J, Jin F, Wang J, Zheng N, Cong Y (2015) Effects of CO2-driven ocean acidification on early life stages of marine medaka (Oryzias melastigma). Biogeosciences 12(12):3861–3868

  76. Munday PL (2014) Transgenerational acclimation of fishes to climate change and ocean acidification. F1000prime Rep 6:99

  77. Munday PL, Crawley NE, Nilsson GE (2009a) Interacting effects of elevated temperature and ocean acidification on the aerobic performance of coral reef fishes. Mar Ecol Prog Ser 388:235–242

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

  79. Munday PL, Donelson JM, Dixson DL, Endo GG (2009c) Effects of ocean acidification on the early life history of a tropical marine fish. Proc Biol Sci 276(1671):3275–3283

  80. Munday PL, Dixson DL, McCormick MI, Meekan M, Ferrari MC, Chivers DP (2010) Replenishment of fish populations is threatened by ocean acidification. Proc Natl Acad Sci USA 107(29):12930–12934

  81. Munday PL, Gagliano M, Donelson JM, Dixson DL, Thorrold SR (2011) Ocean acidification does not affect the early life history development of a tropical marine fish. Mar Ecol Prog Ser 423:211–221

  82. Munday PL, McCormick MI, Nilsson GE (2012) Impact of global warming and rising CO2 levels on coral reef fishes: what hope for the future? J Exp Biol 215(Pt 22):3865–3873

  83. Munday PL, Warner RR, Monro K, Pandolfi JM, Marshall DJ (2013) Predicting evolutionary responses to climate change in the sea. Ecol Lett 16(12):1488–1500

  84. Murray CS, Malvezzi A, Gobler CJ, Baumann H (2014) Offspring sensitivity to ocean acidification changes seasonally in a coastal marine fish. Mar Ecol Prog Ser 504:1–11

  85. Nagelkerken I, Munday PL (2016) Animal behaviour shapes the ecological effects of ocean acidification and warming: moving from individual to community-level responses. Glob Chang Biol 22(3):974–989

  86. Nilsson GE, Lefevre S (2016) Physiological challenges to fishes in a warmer and acidified future. Physiology 31(6):409–417

  87. Nilsson GE, Dixson DL, Domenici P, McCormick MI, Sorensen C, Watson S, Munday PL (2012) Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nat Clim Change 2:201–204

  88. Ou M, Hamilton TJ, Eom J, Lyall EM, Gallup J, Jiang A, Lee J, Close DA, Yun S-S, Brauner CJ (2015) Responses of pink salmon to CO2-induced aquatic acidification. Nature Clim Change 5(10):950–955

  89. Pan TC, Applebaum SL, Manahan DT (2015) Experimental ocean acidification alters the allocation of metabolic energy. Proc Natl Acad Sci USA 112(15):4696–4701

  90. Perry SF (1986) Carbon dioxide excretion in fishes. Can J Zool 64:565–572

  91. Perry SF, Abdallah S (2012) Mechanisms and consequences of carbon dioxide sensing in fish. Respir Physiol Neurobiol 184(3):309–315

  92. 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

  93. Perry SE, Fritsche R, Hoagland TM, Duff DW, Olson KR (1999) The control of blood pressure during external hypercapnia in the rainbow trout (Oncorhynchus mykiss). J Exp Biol 202(16):2177–2190

  94. Perry SF, Braun MH, Genz J, Vulesevic B, Taylor J, Grosell M, Gilmour KM (2010) Acid–base regulation in the plainfin midshipman (Porichthys notatus): an aglomerular marine teleost. J Comp Physiol B 180(8):1213–1225

  95. 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(18):4187–4196

  96. Pfister CA, Esbaugh AJ, Frieder CA, Baumann H, Bockmon EE, White MM, Carter BR, Benway HM, Blanchette CA, Carrington E, McClintock JB, McCorkle DC, McGillis WR, Mooney TA, Ziveri P (2014) Detecting the unexpected: a research framework for ocean acidification. Environ Sci Technol 48(17):9982–9994

  97. Pimentel MS, Faleiro F, Dionisio G, Repolho T, Pousao-Ferreira P, Machado J, Rosa R (2014) Defective skeletogenesis and oversized otoliths in fish early stages in a changing ocean. J Exp Biol 217(Pt 12):2062–2070

  98. Pimentel MS, Faleiro F, Marques T, Bispo R, Dionisio G, Faria AM, Machado J, Peck MA, Portner H, Pousao-Ferreira P, Goncalves EJ, Rosa R (2016) Foraging behaviour, swimming performance and malformations of early stages of commercially important fishes under ocean acidification and warming. Clim Change 137(3–4):495–509

  99. Pope EC, Ellis RP, Scolamacchia M, Scolding JWS, Keay A, Chingombe P, Shields RJ, Wilcox R, Speirs DC, Wilson RW, Lewis C, Flynn KJ (2014) European sea bass, Dicentrarchus labrax, in a changing ocean. Biogeosciences 11(9):2519–2530

  100. Portner HO (2010) Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213(6):881–893

  101. Portner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315(5808):95–97

  102. Putnam HM, Davidson JM, Gates RD (2016) Ocean acidification influences host DNA methylation and phenotypic plasticity in environmentally susceptible corals. Evol Appl 9(9):1165–1178

  103. Randall DJ, Heisler N, Drees F (1976) Ventilatory response to hypercapnia in larger spotted dogfish Scyliorhinus stellaris. Am J Physiol 230(3):590–594

  104. Regan MD, Turko AJ, Heras J, Andersen MK, Lefevre S, Wang T, Bayley M, Brauner CJ, Huong DTT, Phuong NT, Nilsson GE (2016) Ambient CO2, fish behaviour and altered GABAergic neurotransmission: exploring the mechanism of CO2-altered behaviour by taking a hypercapnia dweller down to low CO2 levels. J Exp Biol 219(1):109–118

  105. Rivera C, Voipio J, Payne JA, Ruusuvuori E, Lahtinen H, Lamsa K, Pirvola U, Saarma M, Kaila K (1999) The K+/Cl-co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397(6716):251–255

  106. Rivera C, Voipio J, Kaila K (2005) Two developmental switches in GABAergic signalling: the K+-Cl-cotransporter KCC2 and carbonic anhydrase CAVII. J Physiol 562(Pt 1):27–36

  107. Roche DG, Careau V, Binning SA (2016) Demystifying animal ‘personality’ (or not): why individual variation matters to experimental biologists. J Exp Biol 219(Pt 24):3832–3843

  108. Rosa R, Rummer JL, Munday PL (2017) Biological responses of sharks to ocean acidification. Biol Lett 13(3):20160796

  109. Rossi T, Nagelkerken I, Simpson SD, Pistevos JCA, Watson S-A, Merillet L, Fraser P, Munday PL, Connell SD (2015) Ocean acidification boosts larval fish development but reduces the window of opportunity for successful settlement. Proc R Soc B Biol Sci 282(1821)

  110. Rossi T, Nagelkerken I, Pistevos JC (2016) Lost at sea: ocean acidification undermines larval fish orientation via altered hearing and marine soundscape modification. Biol Lett 12(1):20150937

  111. Rummer JL, Brauner CJ (2011) Plasma-accessible carbonic anhydrase at the tissue of a teleost fish may greatly enhance oxygen delivery: in vitro evidence in rainbow trout, Oncorhynchus mykiss. J Exp Biol 214(Pt 14):2319–2328

  112. Rummer JL, McKenzie DJ, Innocenti A, Supuran CT, Brauner CJ (2013a) Root effect hemoglobin may have evolved to enhance general tissue oxygen delivery. Science 340(6138):1327–1329

  113. Rummer JL, Stecyk JAW, Couturier CS, Watson SA, Nilsson GE, Munday PL (2013b) Elevated CO2 enhances aerobic scope of a coral reef fish. Conserv Physiol 1(1). doi:10.1093/conphys/cot023

  114. Sardella B, Brauner C (2007) The Osmo-respiratory compromise in fish. In: Fish respiration and environment. Science Publishers, Enfield, NH, pp 147–165

  115. Shen SG, Chen F, Schoppik DE, Checkley DM Jr (2016) Otolith size and the vestibulo–ocular reflex of larvae of white seabass Atractoscion nobilis at high pCO2. Mar Ecol Prog Ser 553:173–183

  116. Simpson SD, Meekan M, Montgomery J, McCauley R, Jeffs A (2005) Homeward sound. Science 308(5719):221

  117. 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

  118. Stapp LS, Kreiss CM, Portner HO, Lannig G (2015) Differential impacts of elevated CO2 and acidosis on the energy budget of gill and liver cells from Atlantic cod, Gadus morhua. Comp Biochem Physiol A Mol Integr Physiol 187:160–167

  119. Strobel A, Bennecke S, Leo E, Mintenbeck K, Portner HO, Mark FC (2012) Metabolic shifts in the Antarctic fish Notothenia rossii in response to rising temperature and PCO2. Front Zool 9(1):28

  120. Strobel A, Graeve M, Poertner HO, Mark FC (2013) Mitochondrial acclimation capacities to ocean warming and acidification are limited in the antarctic Nototheniid Fish, Notothenia rossii and Lepidonotothen squamifrons. PLoS One 8(7):e68865

  121. Sunday JM, Pecl GT, Frusher S, Hobday AJ, Hill N, Holbrook NJ, Edgar GJ, Stuart-Smith R, Barrett N, Wernberg T, Watson RA, Smale DA, Fulton EA, Slawinski D, Feng M, Radford BT, Thompson PA, Bates AE (2015) Species traits and climate velocity explain geographic range shifts in an ocean-warming hotspot. Ecol Lett 18(9):944–953

  122. Titz S, Sammler EM, Hormuzdi SG (2015) Could tuning of the inhibitory tone involve graded changes in neuronal chloride transport? Neuropharmacology 95:321–331

  123. Tresguerres M, Hamilton TJ (2017) Acid–base physiology, neurobiology and behaviour in relation to CO2-induced ocean acidification. J Exp Biol (In Press)

  124. Tseng YC, Hu MY, Stumpp M, Lin LY, Melzner F, Hwang PP (2013) CO(2)-driven seawater acidification differentially affects development and molecular plasticity along life history of fish (Oryzias latipes). Comp Biochem Physiol A Mol Integr Physiol 165(2):119–130

  125. Tufts B, Perry SF (1998) Carbon dioxide transport and excretion. In: Fish physiology, vol 17. Fish Respiration. Academic Press, San Diego, pp 229–282

  126. Welch MJ, Munday PL (2016) Contrasting effects of ocean acidification on reproduction in reef fishes. Coral Reefs 35(2):485–493

  127. Zhang RW, Wei HP, Xia YM, Du JL (2010) Development of light response and GABAergic excitation-to-inhibition switch in zebrafish retinal ganglion cells. J Physiol 588(Pt 14):2557–2569

Download references

Acknowledgements

AJE is supported by a National Science Foundation Grant (EF-1315290). The author has no conflict of interests with respect to this work.

Author information

Correspondence to Andrew J. Esbaugh.

Additional information

Communicated by I.D. Hume.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Esbaugh, A.J. Physiological implications of ocean acidification for marine fish: emerging patterns and new insights. J Comp Physiol B 188, 1–13 (2018). https://doi.org/10.1007/s00360-017-1105-6

Download citation

Keywords

  • Climate change
  • Hypercapnia
  • Acidosis
  • Aerobic scope
  • Ionocyte
  • GABAA receptor