1932

Abstract

In the last few decades, numerous studies have investigated the impacts of simulated ocean acidification on marine species and communities, particularly those inhabiting dynamic coastal systems. Despite these research efforts, there are many gaps in our understanding, particularly with respect to physiological mechanisms that lead to pathologies. In this review, we trace how carbonate system disturbances propagate from the coastal environment into marine invertebrates and highlight mechanistic links between these disturbances and organism function. We also point toward several processes related to basic invertebrate biology that are severely understudied and prevent an accurate understanding of how carbonate system dynamics influence organismic homeostasis and fitness-related traits. We recommend that significant research effort be directed to studying cellular phenotypes of invertebrates acclimated or adapted to elevated seawater CO using biochemical and physiological methods.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-marine-010419-010658
2020-01-03
2024-06-23
Loading full text...

Full text loading...

/deliver/fulltext/marine/12/1/annurev-marine-010419-010658.html?itemId=/content/journals/10.1146/annurev-marine-010419-010658&mimeType=html&fmt=ahah

Literature Cited

  1. Abe H. 2000. Role of histidine-related compounds as intracellular proton buffering constituents in vertebrate muscle. Biochemistry (Moscow) 65:757–65
    [Google Scholar]
  2. Acin-Perez R, Salazar E, Kamenetsky M, Buck J, Levin LR, Manfredi G 2009. Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation. Cell Metab 9:265–76
    [Google Scholar]
  3. Allmon EB, Esbaugh AJ. 2017. Carbon dioxide induced plasticity of branchial acid-base pathways in an estuarine teleost. Sci. Rep. 7:45680
    [Google Scholar]
  4. Arias-Hidalgo M, Al-Samir S, Gros G, Endeward V 2018. Cholesterol is the main regulator of the carbon dioxide permeability of biological membranes. Am. J. Physiol. Cell Physiol. 315:C137–40
    [Google Scholar]
  5. Arias-Hidalgo M, Geers-Knorr C, Al-Samir S, Gros G, Endeward V 2016. CO2 permeability of rat ventricular cardiomyocytes. Acta Physiol 216:115–28
    [Google Scholar]
  6. Arias-Hidalgo M, Gros G, Endeward V 2017. CO2 and HCO3 permeability of rat liver mitochondria. Acta Physiol 219:64–66
    [Google Scholar]
  7. Bach LT. 2015. Reconsidering the role of carbonate ion concentration in calcification by marine organisms. Biogeosciences 12:4939–51
    [Google Scholar]
  8. Barott KL, Barron ME, Tresguerres M 2017. Identification of a molecular pH sensor in coral. Proc. R. Soc. B 284:20171769
    [Google Scholar]
  9. Barron ME, Thies AB, Espinoza JA, Barott KL, Hamdoun A, Tresguerres M 2018. A vesicular Na+/Ca2+ exchanger in coral calcifying cells. PLOS ONE 13:e0209734
    [Google Scholar]
  10. 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. Estuaries Coasts 38:220–31
    [Google Scholar]
  11. Baverel G, Lund P. 1979. Role for bicarbonate in the regulation of mammalian glutamine-metabolism. Biochem. J. 184:599–606
    [Google Scholar]
  12. Beltrán C, Vacquier VD, Moy G, Chen YQ, Buck J et al. 2007. Particulate and soluble adenylyl cyclases participate in the sperm acrosome reaction. Biochem. Biophys. Res. Commun. 358:1128–35
    [Google Scholar]
  13. Beniash E, Aizenberg J, Addadi L, Weiner S 1997. Amorphous calcium carbonate transforms into calcite during sea urchin larval spicule growth. Proc. R. Soc. B 264:461–65
    [Google Scholar]
  14. Birk MA, McLean EL, Seibel BA 2018. Ocean acidification does not limit squid metabolism via blood oxygen supply. J. Exp. Biol. 221:jeb187443
    [Google Scholar]
  15. Bleich M, Shan QX, Himmerkus N 2012. Calcium regulation of tight junction permeability. Ann. N.Y. Acad. Sci. 1258:93–99
    [Google Scholar]
  16. Boron WF. 2004. Regulation of intracellular pH. Adv. Physiol. Educ. 28:160–79
    [Google Scholar]
  17. Cai WJ, Hu XP, Huang WJ, Murrell MC, Lehrter JC et al. 2011. Acidification of subsurface coastal waters enhanced by eutrophication. Nat. Geosci. 4:766–70
    [Google Scholar]
  18. Cameron JN, Iwama GK. 1987. Compensation of progressive hypercapnia in channel catfish and blue crabs. J. Exp. Biol. 133:183–97
    [Google Scholar]
  19. Chan NCS, Wangpraseurt D, Kuhl M, Connolly SR 2016. Flow and coral morphology control coral surface pH: implications for the effects of ocean acidification. Front. Mar. Sci. 3:10
    [Google Scholar]
  20. Checkley DM, Dickson AG, Takahashi M, Radich JA, Eisenkolb N, Asch R 2009. Elevated CO2 enhances otolith growth in young fish. Science 324:1683
    [Google Scholar]
  21. Clark D, Lamare M, Barker M 2009. Response of sea urchin pluteus larvae (Echinodermata: Echinoidea) to reduced seawater pH: a comparison among a tropical, temperate, and a polar species. Mar. Biol. 156:1125–37
    [Google Scholar]
  22. Clements JC, Bishop MM, Hunt HL 2017. Elevated temperature has adverse effects on GABA-mediated avoidance behaviour to sediment acidification in a wide-ranging marine bivalve. Mar. Biol. 164:56
    [Google Scholar]
  23. Clements JC, Darrow ES. 2018. Eating in an acidifying ocean: a quantitative review of elevated CO2 effects on the feeding rates of calcifying marine invertebrates. Hydrobiologia 820:1–21
    [Google Scholar]
  24. Cochran RE, Burnett LE. 1996. Respiratory responses of the salt marsh animals, Fundulus heteroclitus, Leiostomus xanthurus, and Palaemonetespugio to environmental hypoxia and hypercapnia and to the organophosphate pesticide, azinphosmethyl. J. Exp. Mar. Biol. Ecol 195:125–44
    [Google Scholar]
  25. Collard M, Laitat K, Moulin L, Catarino AI, Grosjean P, Dubois P 2013. Buffer capacity of the coelomic fluid in echinoderms. Comp. Biochem. Physiol. A 166:199–206
    [Google Scholar]
  26. Cornwall CE, Boyd PW, McGraw CM, Hepburn CD, Pilditch CA et al. 2014. Diffusion boundary layers ameliorate the negative effects of ocean acidification on the temperate coralline macroalga Arthrocardia corymbosa. . PLOS ONE 9:e97235
    [Google Scholar]
  27. Cornwall CE, Hepburn CD, McGraw CM, Currie KI, Pilditch CA et al. 2013. Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. Proc. R. Soc. B 280:20132201
    [Google Scholar]
  28. De Beer D, Larkum AWD 2001. Photosynthesis and calcification in the calcifying algae Halimeda discoidea studied with microsensors. Plant Cell Environ 24:1209–17
    [Google Scholar]
  29. De Wit P, Dupont S, Thor P 2016. Selection on oxidative phosphorylation and ribosomal structure as a multigenerational response to ocean acidification in the common copepod Pseudocalanus acuspes. Evol. Appl 9:1112–23
    [Google Scholar]
  30. Dean JB. 2010. Hypercapnia causes cellular oxidation and nitrosation in addition to acidosis: implications for CO2 chemoreceptor function and dysfunction. J. Appl. Physiol. 108:1786–95
    [Google Scholar]
  31. DeVol RT, Sun CY, Marcus MA, Coppersmith SN, Myneni SCB, Gilbert PUPA 2015. Nanoscale transforming mineral phases in fresh nacre. J. Am. Chem. Soc. 137:13325–33
    [Google Scholar]
  32. Diaz RJ, Rosenberg R. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321:926–29
    [Google Scholar]
  33. 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
    [Google Scholar]
  34. Dodd LF, Grabowski JH, Piehler MF, Westfield I, Ries JB 2015. Ocean acidification impairs crab foraging behaviour. Proc. R. Soc. B 282:20150333
    [Google Scholar]
  35. Dorey N, Lancon P, Thorndyke M, Dupont S 2013. Assessing physiological tipping point of sea urchin larvae exposed to a broad range of pH. Glob. Change Biol. 19:3355–67
    [Google Scholar]
  36. Duarte CM, Krause-Jensen D. 2018. Greenland tidal pools as hot spots for ecosystem metabolism and calcification. Estuaries Coasts 41:1314–21
    [Google Scholar]
  37. Endeward V, Al-Samir S, Itel F, Gros G 2014. How does carbon dioxide permeate cell membranes? A discussion of concepts, results and methods. Front. Physiol. 4:382
    [Google Scholar]
  38. Ern R, Esbaugh AJ. 2016. Hyperventilation and blood acid-base balance in hypercapnia exposed red drum (Sciaenops ocellatus). J. Comp. Physiol. B 186:447–60
    [Google Scholar]
  39. Esbaugh AJ. 2018. Physiological implications of ocean acidification for marine fish: emerging patterns and new insights. J. Comp. Physiol. B 188:1–13
    [Google Scholar]
  40. 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 186:97–109
    [Google Scholar]
  41. Evans TG, Chan F, Menge BA, Hofmann GE 2013. Transcriptomic responses to ocean acidification in larval sea urchins from a naturally variable pH environment. Mol. Ecol. 22:1609–25
    [Google Scholar]
  42. Evans TG, Pespeni MH, Hofmann GE, Palumbi SR, Sanford E 2017. Transcriptomic responses to seawater acidification among sea urchin populations inhabiting a natural pH mosaic. Mol. Ecol. 26:2257–75
    [Google Scholar]
  43. Eyre BD, Cyronak T, Drupp P, De Carlo EH, Sachs JP, Andersson AJ 2018. Coral reefs will transition to net dissolving before end of century. Science 359:908–11
    [Google Scholar]
  44. Fitzer SC, Chung P, Maccherozzi F, Dhesi SS, Kamenos NA et al. 2016. Biomineral shell formation under ocean acidification: a shift from order to chaos. Sci. Rep. 6:21076
    [Google Scholar]
  45. Fitzer SC, Zhu WZ, Tanner KE, Phoenix VR, Kamenos NA, Cusack M 2015. Ocean acidification alters the material properties of Mytilus edulis shells. J. R. Soc. Interface 12:20141227
    [Google Scholar]
  46. Foo SA, Byrne M. 2017. Marine gametes in a changing ocean: impacts of climate change stressors on fecundity and the egg. Mar. Environ. Res. 128:12–24
    [Google Scholar]
  47. Franch HA, Raissi S, Wang XN, Zheng B, Bailey JL, Price SR 2004. Acidosis impairs insulin receptor substrate-1-associated phosphoinositide 3-kinase signaling in muscle cells: consequences on proteolysis. Am. J. Physiol. Renal Physiol. 287:F700–6
    [Google Scholar]
  48. Frieder CA, Applebaum SL, Pan TCF, Hedgecock D, Manahan DT 2017. Metabolic cost of calcification in bivalve larvae under experimental ocean acidification. ICES J. Mar. Sci. 74:941–54
    [Google Scholar]
  49. 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. Change Biol. 20:754–64
    [Google Scholar]
  50. Furuse M, Tsukita S. 2006. Claudins in occluding junctions of humans and flies. Trends Cell Biol 16:181–88
    [Google Scholar]
  51. Geers C, Gros G. 2000. Carbon dioxide transport and carbonic anhydrase in blood and muscle. Physiol. Rev. 80:681–715
    [Google Scholar]
  52. Goncalves P, Anderson K, Thompson EL, Melwani A, Parker LM et al. 2016. Rapid transcriptional acclimation following transgenerational exposure of oysters to ocean acidification. Mol. Ecol. 25:4836–49
    [Google Scholar]
  53. Gutowska MA, Melzner F, Langenbuch M, Bock C, Claireaux G, Pörtner HO 2010a. Acid-base regulatory ability of the cephalopod (Sepia officinalis) in response to environmental hypercapnia. J. Comp. Physiol. B 180:323–35
    [Google Scholar]
  54. Gutowska MA, Melzner F, Pörtner HO, Meier S 2010b. Cuttlebone calcification increases during exposure to elevated seawater pCO2 in the cephalopod Sepiaofficinalis. Mar. Biol 157:1653–63
    [Google Scholar]
  55. Haider F, Falfushynska H, Ivanina AV, Sokolova IM 2016. Effects of pH and bicarbonate on mitochondrial functions of marine bivalves. Comp. Biochem. Physiol. A 198:41–50
    [Google Scholar]
  56. Hardewig I, Pörtner HO, Grieshaber MK 1994. Interactions of anaerobic propionate formation and acid-base status in Arenicola marina: an analysis of propionyl-CoA carboxylase. Physiol. Zool. 67:892–909
    [Google Scholar]
  57. Harms L, Frickenhaus S, Schiffer M, Mark FC, Storch D et al. 2014. Gene expression profiling in gills of the great spider crab Hyas araneus in response to ocean acidification and warming. BMC Genom 15:789
    [Google Scholar]
  58. Harrington MJ, Waite JH. 2007. Holdfast heroics: comparing the molecular and mechanical properties of Mytilus californianus byssal threads. J. Exp. Biol. 210:4307–18
    [Google Scholar]
  59. Hay ME. 2009. Marine chemical ecology: chemical signals and cues structure marine populations, communities, and ecosystems. Annu. Rev. Mar. Sci. 1:193–212
    [Google Scholar]
  60. Hendriks IE, Duarte CM, Marba N, Krause-Jensen D 2017. pH gradients in the diffusive boundary layer of subarctic macrophytes. Polar Biol 40:2343–48
    [Google Scholar]
  61. Heuer RM, Grosell M. 2014. Physiological impacts of elevated carbon dioxide and ocean acidification on fish. Am. J. Physiol. Regul. Integr. Comp. Physiol. 307:R1061–84
    [Google Scholar]
  62. Heuer RM, Grosell M. 2016. Elevated CO2 increases energetic cost and ion movement in the marine fish intestine. Sci. Rep. 6:34480
    [Google Scholar]
  63. Hiebenthal C, Fietzek P, Thomsen J, Saderne V, Melzner F 2016. Kiel Fjord pCO2 datasets between 2012 (July) and 2015 (January) measured using a HydroC® pCO2 sensor Data Set, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Ger. https://doi.org/10.1594/PANGAEA.859407
    [Crossref] [Google Scholar]
  64. Hofmann AF, Peltzer ET, Brewer PG 2013. Kinetic bottlenecks to chemical exchange rates for deep-sea animals – part 2: carbon dioxide. Biogeosciences 10:2409–25
    [Google Scholar]
  65. Holtmann WC, Stumpp M, Gutowska MA, Syre S, Himmerkus N et al. 2013. Maintenance of coelomic fluid pH in sea urchins exposed to elevated CO2: the role of body cavity epithelia and stereom dissolution. Mar. Biol. 160:2631–45
    [Google Scholar]
  66. Hu MY, Guh YJ, Stumpp M, Lee JR, Chen RD et al. 2014. Branchial NH4+-dependent acid-base transport mechanisms and energy metabolism of squid (Sepioteuthis lessoniana) affected by seawater acidification. Front. Zool. 11:55
    [Google Scholar]
  67. Hu MY, Tseng YC, Stumpp M, Gutowska MA, Kiko R et al. 2011. Elevated seawater Pco2 differentially affects branchial acid-base transporters over the course of development in the cephalopod Sepia officinalis. Am. J. Physiol. Regul. Integr. Comp. Physiol 301:R1100–14
    [Google Scholar]
  68. Hu MY, Tseng YC, Su YH, Lein E, Lee HG et al. 2017. Variability in larval gut pH regulation defines sensitivity to ocean acidification in six species of the Ambulacraria superphylum. Proc. R. Soc. B 284:20171066
    [Google Scholar]
  69. Hu MY, Yan JJ, Petersen I, Himmerkus N, Bleich M, Stumpp M 2018. A SLC4 family bicarbonate transporter is critical for intracellular pH regulation and biomineralization in sea urchin embryos. eLife 7:e36600
    [Google Scholar]
  70. IPCC (Intergov. Panel Clim. Change) 2014. Climate Change 2014: Impacts, Adaptation, and Vulnerability, Part A: Global and Sectoral Aspects: Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change Ed. CB Field, VR Barros, DJ Dokken, KJ Mach, MD Mastrandrea et al. Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  71. Ivanina AV, Falfushynska HI, Beniash E, Piontkivska H, Sokolova IM 2017. Biomineralization-related specialization of hemocytes and mantle tissues of the Pacific oyster Crassostrea gigas. J. Exp. Biol 220:3209–21
    [Google Scholar]
  72. Ivanina AV, Hawkins C, Beniash E, Sokolova IM 2015. Effects of environmental hypercapnia and metal (Cd and Cu) exposure on acid-base and metal homeostasis of marine bivalves. Comp. Biochem. Phys. C 174:1–12
    [Google Scholar]
  73. Jaeckle W. 2017. Physiology of larval feeding. Evolutionary Ecology of Marine Invertebrate Larvae T Carrier, A Reitzel, A Heyland A 124–41 Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  74. Johnson KM, Hofmann GE. 2017. Transcriptomic response of the Antarctic pteropod Limacina helicina antarctica to ocean acidification. BMC Genom 18:812
    [Google Scholar]
  75. Jonusaite S, Donini A, Kelly SP 2016. Occluding junctions of invertebrate epithelia. J. Comp. Physiol. B 186:17–43
    [Google Scholar]
  76. Knapp JL, Bridges CR, Krohn J, Hoffman LC, Auerswald L 2015. Acid-base balance and changes in haemolymph properties of the South African rock lobsters, Jasus lalandii, a palinurid decapod, during chronic hypercapnia. Biochem. Biophys. Res. Commun. 461:475–80
    [Google Scholar]
  77. Koh CZY, Hiong KC, Choo CYL, Boo MV, Wong WP et al. 2018. Molecular characterization of a dual domain carbonic anhydrase from the ctenidium of the giant clam, Tridacna squamosa, and its expression levels after light exposure, cellular localization, and possible role in the uptake of exogenous inorganic carbon. Front. Physiol. 9:281
    [Google Scholar]
  78. Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L et al. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Change Biol. 19:1884–96
    [Google Scholar]
  79. Kwiatkowski L, Gaylord B, Hill T, Hosfelt J, Kroeker KJ et al. 2016. Nighttime dissolution in a temperate coastal ocean ecosystem increases under acidification. Sci. Rep. 6:22984
    [Google Scholar]
  80. Larsen BK, Portner HO, Jensen FB 1997. Extra- and intracellular acid-base balance and ionic regulation in cod (Gadus morhua) during combined and isolated exposures to hypercapnia and copper. Mar. Biol. 128:337–46
    [Google Scholar]
  81. Lee K, Tong LT, Millero FJ, Sabine CL, Dickson AG et al. 2006. Global relationships of total alkalinity with salinity and temperature in surface waters of the world's oceans. Geophys. Res. Lett. 33:L19605
    [Google Scholar]
  82. 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:cow009
    [Google Scholar]
  83. Lin TY, Liao BK, Horng JL, Yan JJ, Hsiao CD, Hwang PP 2008. Carbonic anhydrase 2-like a and 15a are involved in acid-base regulation and Na+ uptake in zebrafish H+-ATPase-rich cells. Am. J. Physiol. Cell Physiol. 294:C1250–60
    [Google Scholar]
  84. Lopes AR, Borges FO, Figueiredo C, Sampaio E, Diniz M et al. 2019. Transgenerational exposure to ocean acidification induces biochemical distress in a keystone amphipod species (Gammarus locusta). Environ. Res. 170:168–77
    [Google Scholar]
  85. Maas AE, Lawson GL, Bergan AJ, Tarrant AM 2018. Exposure to CO2 influences metabolism, calcification and gene expression of the thecosome pteropod Limacina retroversa. . J. Exp. Biol 221:jeb164400
    [Google Scholar]
  86. 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 284:20171642
    [Google Scholar]
  87. Mass T, Giuffre AJ, Sun CY, Stifler CA, Frazier MJ et al. 2017. Amorphous calcium carbonate particles form coral skeletons. PNAS 114:E7670–78
    [Google Scholar]
  88. Maus B, Bock C, Pörtner HO 2018. Water bicarbonate modulates the response of the shore crab Carcinus maenas to ocean acidification. J. Comp. Physiol. B 188:749–64
    [Google Scholar]
  89. Mehrbach C, Culberso CH, Hawley JE, Pytkowic RM 1973. Measurement of apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol. Oceanogr. 18:897–907
    [Google Scholar]
  90. Melzner F, Gutowska MA, Langenbuch M, Dupont S, Lucassen M et al. 2009. Physiological basis for high CO2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny?. Biogeosciences 6:2313–31
    [Google Scholar]
  91. Melzner F, Stange P, Trubenbach K, Thomsen J, Casties I et al. 2011. Food supply and seawater pCO2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis. . PLOS ONE 6:e24223
    [Google Scholar]
  92. Melzner F, Thomsen J, Koeve W, Oschlies A, Gutowska MA et al. 2013. Future ocean acidification will be amplified by hypoxia in coastal habitats. Mar. Biol. 160:1875–88
    [Google Scholar]
  93. Michaelidis B, Ouzounis C, Paleras A, Pörtner HO 2005. Effects of long-term moderate hypercapnia on acid-base balance and growth rate in marine mussels Mytilus galloprovincialis. Mar. Ecol. Prog. Ser 293:109–18
    [Google Scholar]
  94. Moya A, Howes EL, Lacoue-Labarthe T, Foret S, Hanna B et al. 2016. Near-future pH conditions severely impact calcification, metabolism and the nervous system in the pteropod Heliconoides inflatus. Glob. Change Biol. 22:3888–900
    [Google Scholar]
  95. Munday PL, Dixson DL, Donelson JM, Jones GP, Pratchett MS et al. 2009. Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. PNAS 106:1848–52
    [Google Scholar]
  96. Nagelkerken I, Munday PL. 2016. Animal behaviour shapes the ecological effects of ocean acidification and warming: moving from individual to community-level responses. Glob. Change Biol. 22:974–89
    [Google Scholar]
  97. Nienhuis S, Palmer AR, Harley CDG 2010. Elevated CO2 affects shell dissolution rate but not calcification rate in a marine snail. Proc. R. Soc. B 277:2553–58
    [Google Scholar]
  98. Nilsson GE, Dixson DL, Domenici P, McCormick MI, Sorensen C et al. 2012. Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nat. Clim. Change 2:201–4
    [Google Scholar]
  99. O'Donnell MJ, George MN, Carrington E 2013. Mussel byssus attachment weakened by ocean acidification. Nat. Clim. Change 3:587–90
    [Google Scholar]
  100. Oeschger R. 1990. Long-term anaerobiosis in sublittoral marine-invertebrates from the western Baltic Sea: Halicryptus spinulosus (Priapulida), Astarte borealis and Arctica islandica (Bivalvia). Mar. Ecol. Prog. Ser. 59:133–43
    [Google Scholar]
  101. Pan TCF, Applebaum SL, Manahan DT 2015. Experimental ocean acidification alters the allocation of metabolic energy. PNAS 112:4696–701
    [Google Scholar]
  102. Pane EF, Barry JP. 2007. Extracellular acid-base regulation during short-term hypercapnia is effective in a shallow-water crab, but ineffective in a deep-sea crab. Mar. Ecol. Prog. Ser. 334:1–9
    [Google Scholar]
  103. Pansch C, Hiebenthal C. 2019. A new mesocosm system to study the effects of environmental variability on marine species and communities. Limnol. Oceanogr. Methods 17:145–62
    [Google Scholar]
  104. Peck VL, Oakes RL, Harper EM, Manno C, Tarling GA 2018. Pteropods counter mechanical damage and dissolution through extensive shell repair. Nat. Commun. 9:264
    [Google Scholar]
  105. Pespeni MH, Sanford E, Gaylord B, Hill TM, Hosfelt JD et al. 2013. Evolutionary change during experimental ocean acidification. PNAS 110:6937–42
    [Google Scholar]
  106. Piermarini PM, Choi I, Boron WF 2007. Cloning and characterization of an electrogenic Na/HCO3 cotransporter from the squid giant fiber lobe. Am. J. Physiol. Cell Physiol. 292:C2032–45
    [Google Scholar]
  107. Politi Y, Arad T, Klein E, Weiner S, Addadi L 2004. Sea urchin spine calcite forms via a transient amorphous calcium carbonate phase. Science 306:1161–64
    [Google Scholar]
  108. Porteus CS, Hubbard PC, Webster TMU, van Aerie R, Canario AVM et al. 2018. Near-future CO2 levels impair the olfactory system of a marine fish. Nat. Clim. Change 8:737–43
    [Google Scholar]
  109. Pörtner HO. 1990. Determination of intracellular buffer values after metabolic inhibition by fluoride and nitrilotriacetic acid. Respir. Physiol. 81:275–88
    [Google Scholar]
  110. Pörtner HO, Boutilier RG, Tang Y, Toews DP 1990. Determination of intracellular pH and PCO2 after metabolic inhibition by fluoride and nitrilotriacetic acid. Respir. Physiol. 81:255–73
    [Google Scholar]
  111. Pörtner HO, Reipschläger A, Heisler N 1998. Acid-base regulation, metabolism and energetics in Sipunculus nudus as a function of ambient carbon dioxide level. J. Exp. Biol. 201:43–55
    [Google Scholar]
  112. Pörtner HO, Sartoris FJ. 1999. Invasive studies of intracellular acid-base parameters: environmental and functional aspects. Regulation of Tissue pH in Plants and Animals: A Reappraisal of Current Techniques S Egginton, EW Taylor, JA Raven 69–98 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  113. Pörtner HO, Webber DM, Boutilier RG, O'Dor RK 1991. Acid-base regulation in exercising squid (Illex illecebrosus, Loligo pealei). Am. J. Physiol. 261:R239–46
    [Google Scholar]
  114. Ramesh K, Hu MY, Thomsen J, Bleich M, Melzner F 2017. Mussel larvae modify calcifying fluid carbonate chemistry to promote calcification. Nat. Commun. 8:1709
    [Google Scholar]
  115. Ramesh K, Melzner F, Griffith AW, Gobler CJ, Rouger C et al. 2018. In vivo characterization of bivalve larval shells: a confocal Raman microscopy study. J. R. Soc. Interface 15:20170723
    [Google Scholar]
  116. Reipschläger A, Pörtner HO. 1996. Metabolic depression during environmental stress: the role of extracellular versus intracellular pH in Sipunculus nudus. J. Exp. Biol 199:1801–7
    [Google Scholar]
  117. Ries JB, Ghazaleh MN, Connolly B, Westfield I, Castillo KD 2016. Impacts of seawater saturation state (ΩA = 0.4–4.6) and temperature (10, 25 °C) on the dissolution kinetics of whole-shell biogenic carbonates. Geochim. Cosmochim. Acta 192:318–37
    [Google Scholar]
  118. Roggatz CC, Lorch M, Hardege JD, Benoit DM 2016. Ocean acidification affects marine chemical communication by changing structure and function of peptide signalling molecules. Glob. Change Biol. 22:3914–26
    [Google Scholar]
  119. Rosa R, Seibel BA. 2008. Synergistic effects of climate-related variables suggest future physiological impairment in a top oceanic predator. PNAS 105:20776–80
    [Google Scholar]
  120. Saderne V, Fietzek P, Herman PMJ 2013. Extreme variations of pCO2 and pH in a macrophyte meadow of the Baltic Sea in summer: evidence of the effect of photosynthesis and local upwelling. PLOS ONE 8:e62689
    [Google Scholar]
  121. Saleuddin ASM, Petit HP. 1983. The mode of formation and the structure of the periostracum. The Mollusca, Vol. 4:Physiology: Part 1 ASM Saleuddin, KM Wilbur 199–234 New York: Academic
    [Google Scholar]
  122. Santo-Domingo J, Demaurex N. 2012. The renaissance of mitochondrial pH. J. Gen. Physiol. 139:415–23
    [Google Scholar]
  123. Semmens DC, Dane RE, Pancholi MR, Slade SE, Scrivens JH, Elphick MR 2013. Discovery of a novel neurophysin-associated neuropeptide that triggers cardiac stomach contraction and retraction in starfish. J. Exp. Biol. 216:4047–53
    [Google Scholar]
  124. Sevilgen DS, Venn AA, Hu MY, Tambutte E, de Beer D et al. 2019. Full in vivo characterization of carbonate chemistry at the site of calcification in corals. Sci. Adv. 5:eaau7447
    [Google Scholar]
  125. Sibony-Nevo O, Pinkas I, Farstey V, Baron H, Addadi L, Weiner S 2019. The pteropod Creseis acicula forms its shell through a disordered nascent aragonite phase. Crystal Growth Design 19:2564–73
    [Google Scholar]
  126. Sillanpaa JK, Sundh H, Sundell KS 2018. Calcium transfer across the outer mantle epithelium in the Pacific oyster, Crassostrea gigas. Proc. R. Soc. B 285:20181676
    [Google Scholar]
  127. Simpson DP. 1967. Regulation of renal citrate metabolism by bicarbonate ion and pH: observations in tissue slices and mitochondria. J. Clin. Investig. 46:225–38
    [Google Scholar]
  128. Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA 2012. Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar. Environ. Res. 79:1–15
    [Google Scholar]
  129. Spady BL, Munday PL, Watson SA 2018. Predatory strategies and behaviours in cephalopods are altered by elevated CO2. Glob. Change Biol. 24:2585–96
    [Google Scholar]
  130. Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U et al. 2008. The Trichoplax genome and the nature of placozoans. Nature 454:955–60
    [Google Scholar]
  131. Steffensen JF. 1989. Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiol. Biochem. 6:49–59
    [Google Scholar]
  132. Strobel A, Bennecke S, Leo E, Mintenbeck K, Pörtner HO, Mark FC 2012. Metabolic shifts in the Antarctic fish Notothenia rossii in response to rising temperature and PCO2. Front. Zool. 9:28
    [Google Scholar]
  133. Stumpp M, Hu MY, Casties I, Saborowski R, Bleich M et al. 2013. Digestion in sea urchin larvae impaired under ocean acidification. Nat. Clim. Change 3:1044–49
    [Google Scholar]
  134. Stumpp M, Hu MY, Melzner F, Gutowska MA, Dorey N et al. 2012a. Acidified seawater impacts sea urchin larvae pH regulatory systems relevant for calcification. PNAS 109:18192–97
    [Google Scholar]
  135. Stumpp M, Hu MY, Tseng YC, Guh YJ, Chen YC et al. 2015. Evolution of extreme stomach pH in bilateria inferred from gastric alkalization mechanisms in basal deuterostomes. Sci. Rep. 5:10421
    [Google Scholar]
  136. Stumpp M, Trubenbach K, Brennecke D, Hu MY, Melzner F 2012b. Resource allocation and extracellular acid-base status in the sea urchin Strongylocentrotus droebachiensis in response to CO2 induced seawater acidification. Aquat. Toxicol. 110:194–207
    [Google Scholar]
  137. Stumpp M, Wren J, Melzner F, Thorndyke MC, Dupont ST 2011. CO2 induced seawater acidification impacts sea urchin larval development I: Elevated metabolic rates decrease scope for growth and induce developmental delay. Comp. Biochem. Physiol. A 160:331–40
    [Google Scholar]
  138. Sutton AJ, Sabine CL, Dietrich C, Maenner Jones S, Musielewicz S et al. 2012. High-resolution ocean and atmosphere pCO2 time-series measurements from mooring WHOTS_158W_23N (NCEI Accession 0100080) Data Set, Natl. Cent. Environ. Inf., Natl. Ocean. Atmos. Adm., Silver Spring, MD. https://doi.org/10.3334/cdiac/otg.tsm_whots
    [Crossref] [Google Scholar]
  139. Tambutte E, Tambutte S, Segonds N, Zoccola D, Venn A et al. 2012. Calcein labelling and electrophysiology: insights on coral tissue permeability and calcification. Proc. R. Soc. B 279:19–27
    [Google Scholar]
  140. Thompson EL, Parker L, Amaral V, Bishop MJ, O'Connor WA, Raftos DA 2016. Wild populations of Sydney rock oysters differ in their proteomic responses to elevated carbon dioxide. Mar. Freshw. Res. 67:1964–72
    [Google Scholar]
  141. Thomsen J, Gutowska MA, Saphörster J, Heinemann A, Trübenbach K et al. 2010. Calcifying invertebrates succeed in a naturally CO2-rich coastal habitat but are threatened by high levels of future acidification. Biogeosciences 7:3879–91
    [Google Scholar]
  142. Thomsen J, Haynert K, Wegner KM, Melzner F 2015. Impact of seawater carbonate chemistry on the calcification of marine bivalves. Biogeosciences 12:4209–20
    [Google Scholar]
  143. Thomsen J, Stapp LS, Haynert K, Schade H, Danelli M et al. 2017. Naturally acidified habitat selects for ocean acidification-tolerant mussels. Sci. Adv. 3:e1602411
    [Google Scholar]
  144. Tohse H, Mugiya Y. 2001. Effects of enzyme and anion transport inhibitors on in vitro incorporation of inorganic carbon and calcium into endolymph and otoliths in salmon Oncorhynchus masou. Comp. Biochem. Physiol. A 128:177–84
    [Google Scholar]
  145. Tomanek L. 2015. Proteomic responses to environmentally induced oxidative stress. J. Exp. Biol. 218:1867–79
    [Google Scholar]
  146. Tomanek L, Zuzow MJ, Ivanina AV, Beniash E, Sokolova IM 2011. Proteomic response to elevated PCO2 level in eastern oysters, Crassostrea virginica: evidence for oxidative stress. J. Exp. Biol. 214:1836–44
    [Google Scholar]
  147. Tresguerres M. 2016. Novel and potential physiological roles of vacuolar-type H+-ATPase in marine organisms. J. Exp. Biol. 219:2088–97
    [Google Scholar]
  148. Tresguerres M, Barott KL, Barron ME, Roa JN 2014. Established and potential physiological roles of bicarbonate-sensing soluble adenylyl cyclase (sAC) in aquatic animals. J. Exp. Biol. 217:663–72
    [Google Scholar]
  149. Tresguerres M, Hamilton TJ. 2017. Acid base physiology, neurobiology and behaviour in relation to CO2-induced ocean acidification. J. Exp. Biol. 220:2136–48
    [Google Scholar]
  150. Trivedi B, Danforth WH. 1966. Effect of pH on kinetics of frog muscle phosphofructokinase. J. Biol. Chem. 241:4110–12
    [Google Scholar]
  151. Truchot JP, Duhameljouve A. 1980. Oxygen and carbon dioxide in the marine intertidal environment: diurnal and tidal changes in rockpools. Respir. Physiol. 39:241–54
    [Google Scholar]
  152. Tunnicliffe V, Davies KTA, Butterfield DA, Embley RW, Rose JM, Chadwick WW 2009. Survival of mussels in extremely acidic waters on a submarine volcano. Nat. Geosci 2:344–48
    [Google Scholar]
  153. Velez Z, Roggatz CC, Benoit DM, Hardege JD, Hubbard PC 2019. Short- and medium-term exposure to ocean acidification reduces olfactory sensitivity in gilthead seabream. Front. Physiol. 10:731
    [Google Scholar]
  154. Wahl M, Covacha SS, Saderne V, Hiebenthal C, Muller JD et al. 2018. Macroalgae may mitigate ocean acidification effects on mussel calcification by increasing pH and its fluctuations. Limnol. Oceanogr. 63:3–21
    [Google Scholar]
  155. 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
    [Google Scholar]
  156. Waldbusser GG, Brunner EL, Haley BA, Hales B, Langdon CJ, Prahl FG 2013. A developmental and energetic basis linking larval oyster shell formation to acidification sensitivity. Geophys. Res. Lett. 40:2171–76
    [Google Scholar]
  157. Waldbusser GG, Hales B, Langdon CJ, Haley BA, Schrader P et al. 2015a. Ocean acidification has multiple modes of action on bivalve larvae. PLOS ONE 10:e012837
    [Google Scholar]
  158. Waldbusser GG, Hales B, Langdon CJ, Haley BA, Schrader P et al. 2015b. Saturation-state sensitivity of marine bivalve larvae to ocean acidification. Nat. Clim. Change 5:273–80
    [Google Scholar]
  159. Waldbusser GG, Salisbury JE. 2014. Ocean acidification in the coastal zone from an organism's perspective: multiple system parameters, frequency domains, and habitats. Annu. Rev. Mar. Sci. 6:221–47
    [Google Scholar]
  160. Wallace RB, Baumann H, Grear JS, Aller RC, Gobler CJ 2014. Coastal ocean acidification: the other eutrophication problem. Estuar. Coast. Shelf Sci. 148:1–13
    [Google Scholar]
  161. Wanders RJA, Meijer AJ, Groen AK, Tager JM 1983. Bicarbonate and the pathway of glutamate oxidation in isolated rat-liver mitochondria. Eur. J. Biochem. 133:245–54
    [Google Scholar]
  162. Watson SA, Lefevre S, McCormick MI, Domenici P, Nilsson GE, Munday PL 2014. Marine mollusc predator-escape behaviour altered by near-future carbon dioxide levels. Proc. R. Soc. B 281:20132377
    [Google Scholar]
  163. Weihrauch D, O'Donnell M, eds. 2017. Acid-Base Balance and Nitrogen Excretion in Invertebrates: Mechanisms and Strategies in Various Invertebrate Groups with Considerations of Challenges Caused by Ocean Acidification Cham, Switz: Springer
    [Google Scholar]
  164. Whiteley NM. 2011. Physiological and ecological responses of crustaceans to ocean acidification. Mar. Ecol. Prog. Ser. 430:257–71
    [Google Scholar]
  165. Wicks LC, Roberts JM. 2012. Benthic invertebrates in a high-CO2 world. Oceanogr. Mar. Biol. Annu. Rev. 50:127–87
    [Google Scholar]
  166. Wong JM, Johnson KM, Kelly MW, Hofmann G 2018. Transcriptomics reveal transgenerational effects in purple sea urchin embryos: Adult acclimation to upwelling conditions alters the response of their progeny to differential pCO2 levels. Mol. Ecol. 27:1120–37
    [Google Scholar]
  167. Wood HL, Spicer JI, Widdicombe S 2008. Ocean acidification may increase calcification rates, but at a cost. Proc. R. Soc. B 275:1767–73
    [Google Scholar]
  168. Wyatt TD, Hardege JD, Terschak J 2014. Ocean acidification foils chemical signals. Science 346:176
    [Google Scholar]
  169. Young CS, Gobler CJ. 2018. The ability of macroalgae to mitigate the negative effects of ocean acidification on four species of North Atlantic bivalve. Biogeosciences 15:6167–83
    [Google Scholar]
/content/journals/10.1146/annurev-marine-010419-010658
Loading
/content/journals/10.1146/annurev-marine-010419-010658
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error