Can variable pH and low oxygen moderate ocean acidification outcomes for mussel larvae?

Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O₂]) levels. In controlled‐laboratory experiments we explored the interactive effects of pH, [O₂], and semidiurnal pH fluctuations on the survivorship, development, and size o...

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Published inGlobal change biology Vol. 20; no. 3; pp. 754 - 764
Main Authors Frieder, Christina A, Gonzalez, Jennifer P, Bockmon, Emily E, Navarro, Michael O, Levin, Lisa A
Format Journal Article
LanguageEnglish
Published Oxford Blackwell Science 01.03.2014
Blackwell Publishing Ltd
Wiley-Blackwell
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Abstract Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O₂]) levels. In controlled‐laboratory experiments we explored the interactive effects of pH, [O₂], and semidiurnal pH fluctuations on the survivorship, development, and size of early life stages of two mytilid mussels, Mytilus californianus and M. galloprovincialis. Survivorship of larvae was unaffected by low pH, low [O₂], or semidiurnal fluctuations for both mytilid species. Low pH (<7.6) resulted in delayed transition from the trochophore to veliger stage, but this effect of low pH was absent when incorporating semidiurnal fluctuations in both species. Also at low pH, larval shells were smaller and had greater variance; this effect was absent when semidiurnal fluctuations of 0.3 units were incorporated at low pH for M. galloprovincialis but not for M. californianus. Low [O₂] in combination with low pH had no effect on larval development and size, indicating that early life stages of mytilid mussels are largely tolerant to a broad range of [O₂] reflective of their environment (80–260 μmol kg⁻¹). The role of pH variability should be recognized as an important feature in coastal oceans that has the capacity to modulate the effects of ocean acidification on biological responses.
AbstractList Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O 2 ]) levels. In controlled‐laboratory experiments we explored the interactive effects of pH , [O 2 ], and semidiurnal pH fluctuations on the survivorship, development, and size of early life stages of two mytilid mussels, Mytilus californianus and M. galloprovincialis . Survivorship of larvae was unaffected by low pH , low [O 2 ], or semidiurnal fluctuations for both mytilid species. Low pH (<7.6) resulted in delayed transition from the trochophore to veliger stage, but this effect of low pH was absent when incorporating semidiurnal fluctuations in both species. Also at low pH , larval shells were smaller and had greater variance; this effect was absent when semidiurnal fluctuations of 0.3 units were incorporated at low pH for M. galloprovincialis but not for M. californianus . Low [O 2 ] in combination with low pH had no effect on larval development and size, indicating that early life stages of mytilid mussels are largely tolerant to a broad range of [O 2 ] reflective of their environment (80–260  μ mol kg −1 ). The role of pH variability should be recognized as an important feature in coastal oceans that has the capacity to modulate the effects of ocean acidification on biological responses.
Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O₂]) levels. In controlled‐laboratory experiments we explored the interactive effects of pH, [O₂], and semidiurnal pH fluctuations on the survivorship, development, and size of early life stages of two mytilid mussels, Mytilus californianus and M. galloprovincialis. Survivorship of larvae was unaffected by low pH, low [O₂], or semidiurnal fluctuations for both mytilid species. Low pH (<7.6) resulted in delayed transition from the trochophore to veliger stage, but this effect of low pH was absent when incorporating semidiurnal fluctuations in both species. Also at low pH, larval shells were smaller and had greater variance; this effect was absent when semidiurnal fluctuations of 0.3 units were incorporated at low pH for M. galloprovincialis but not for M. californianus. Low [O₂] in combination with low pH had no effect on larval development and size, indicating that early life stages of mytilid mussels are largely tolerant to a broad range of [O₂] reflective of their environment (80–260 μmol kg⁻¹). The role of pH variability should be recognized as an important feature in coastal oceans that has the capacity to modulate the effects of ocean acidification on biological responses.
Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O2]) levels. In controlled-laboratory experiments we explored the interactive effects of pH, [O2], and semidiurnal pH fluctuations on the survivorship, development, and size of early life stages of two mytilid mussels, Mytilus californianus and M. galloprovincialis. Survivorship of larvae was unaffected by low pH, low [O2], or semidiurnal fluctuations for both mytilid species. Low pH (<7.6) resulted in delayed transition from the trochophore to veliger stage, but this effect of low pH was absent when incorporating semidiurnal fluctuations in both species. Also at low pH, larval shells were smaller and had greater variance; this effect was absent when semidiurnal fluctuations of 0.3 units were incorporated at low pH for M. galloprovincialis but not for M. californianus. Low [O2] in combination with low pH had no effect on larval development and size, indicating that early life stages of mytilid mussels are largely tolerant to a broad range of [O2] reflective of their environment (80-260 µmol kg-1). The role of pH variability should be recognized as an important feature in coastal oceans that has the capacity to modulate the effects of ocean acidification on biological responses. [PUBLICATION ABSTRACT]
Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O sub(2)]) levels. In controlled-laboratory experiments we explored the interactive effects of pH, [O sub(2)], and semidiurnal pH fluctuations on the survivorship, development, and size of early life stages of two mytilid mussels, Mytilus californianus and M. galloprovincialis. Survivorship of larvae was unaffected by low pH, low [O sub(2)], or semidiurnal fluctuations for both mytilid species. Low pH (<7.6) resulted in delayed transition from the trochophore to veliger stage, but this effect of low pH was absent when incorporating semidiurnal fluctuations in both species. Also at low pH, larval shells were smaller and had greater variance; this effect was absent when semidiurnal fluctuations of 0.3 units were incorporated at low pH for M. galloprovincialis but not for M. californianus. Low [O sub(2)] in combination with low pH had no effect on larval development and size, indicating that early life stages of mytilid mussels are largely tolerant to a broad range of [O sub(2)] reflective of their environment (80-260 mu mol kg super(-1)). The role of pH variability should be recognized as an important feature in coastal oceans that has the capacity to modulate the effects of ocean acidification on biological responses.
Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O2 ]) levels. In controlled-laboratory experiments we explored the interactive effects of pH, [O2 ], and semidiurnal pH fluctuations on the survivorship, development, and size of early life stages of two mytilid mussels, Mytilus californianus and M. galloprovincialis. Survivorship of larvae was unaffected by low pH, low [O2 ], or semidiurnal fluctuations for both mytilid species. Low pH (<7.6) resulted in delayed transition from the trochophore to veliger stage, but this effect of low pH was absent when incorporating semidiurnal fluctuations in both species. Also at low pH, larval shells were smaller and had greater variance; this effect was absent when semidiurnal fluctuations of 0.3 units were incorporated at low pH for M. galloprovincialis but not for M. californianus. Low [O2 ] in combination with low pH had no effect on larval development and size, indicating that early life stages of mytilid mussels are largely tolerant to a broad range of [O2 ] reflective of their environment (80-260 μmol kg(-1) ). The role of pH variability should be recognized as an important feature in coastal oceans that has the capacity to modulate the effects of ocean acidification on biological responses.Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O2 ]) levels. In controlled-laboratory experiments we explored the interactive effects of pH, [O2 ], and semidiurnal pH fluctuations on the survivorship, development, and size of early life stages of two mytilid mussels, Mytilus californianus and M. galloprovincialis. Survivorship of larvae was unaffected by low pH, low [O2 ], or semidiurnal fluctuations for both mytilid species. Low pH (<7.6) resulted in delayed transition from the trochophore to veliger stage, but this effect of low pH was absent when incorporating semidiurnal fluctuations in both species. Also at low pH, larval shells were smaller and had greater variance; this effect was absent when semidiurnal fluctuations of 0.3 units were incorporated at low pH for M. galloprovincialis but not for M. californianus. Low [O2 ] in combination with low pH had no effect on larval development and size, indicating that early life stages of mytilid mussels are largely tolerant to a broad range of [O2 ] reflective of their environment (80-260 μmol kg(-1) ). The role of pH variability should be recognized as an important feature in coastal oceans that has the capacity to modulate the effects of ocean acidification on biological responses.
Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O2]) levels. In controlled‐laboratory experiments we explored the interactive effects of pH, [O2], and semidiurnal pH fluctuations on the survivorship, development, and size of early life stages of two mytilid mussels, Mytilus californianus and M. galloprovincialis. Survivorship of larvae was unaffected by low pH, low [O2], or semidiurnal fluctuations for both mytilid species. Low pH (<7.6) resulted in delayed transition from the trochophore to veliger stage, but this effect of low pH was absent when incorporating semidiurnal fluctuations in both species. Also at low pH, larval shells were smaller and had greater variance; this effect was absent when semidiurnal fluctuations of 0.3 units were incorporated at low pH for M. galloprovincialis but not for M. californianus. Low [O2] in combination with low pH had no effect on larval development and size, indicating that early life stages of mytilid mussels are largely tolerant to a broad range of [O2] reflective of their environment (80–260 μmol kg−1). The role of pH variability should be recognized as an important feature in coastal oceans that has the capacity to modulate the effects of ocean acidification on biological responses.
Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O2 ]) levels. In controlled-laboratory experiments we explored the interactive effects of pH, [O2 ], and semidiurnal pH fluctuations on the survivorship, development, and size of early life stages of two mytilid mussels, Mytilus californianus and M. galloprovincialis. Survivorship of larvae was unaffected by low pH, low [O2 ], or semidiurnal fluctuations for both mytilid species. Low pH (<7.6) resulted in delayed transition from the trochophore to veliger stage, but this effect of low pH was absent when incorporating semidiurnal fluctuations in both species. Also at low pH, larval shells were smaller and had greater variance; this effect was absent when semidiurnal fluctuations of 0.3 units were incorporated at low pH for M. galloprovincialis but not for M. californianus. Low [O2 ] in combination with low pH had no effect on larval development and size, indicating that early life stages of mytilid mussels are largely tolerant to a broad range of [O2 ] reflective of their environment (80-260 μmol kg(-1) ). The role of pH variability should be recognized as an important feature in coastal oceans that has the capacity to modulate the effects of ocean acidification on biological responses.
Author Navarro, Michael O.
Levin, Lisa A.
Frieder, Christina A.
Gonzalez, Jennifer P.
Bockmon, Emily E.
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https://www.ncbi.nlm.nih.gov/pubmed/24343909$$D View this record in MEDLINE/PubMed
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1365-2486
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IsPeerReviewed true
IsScholarly true
Issue 3
Keywords Fluctuations
Oxygen
Variable
multistressor
Acidification
mussel
Larva
Plankton
Bivalvia
coastal variability
pH
planktonic larvae
Ocean
Invertebrata
Mollusca
semidiurnal pH fluctuations
Language English
License http://onlinelibrary.wiley.com/termsAndConditions#vor
CC BY 4.0
2013 John Wiley & Sons Ltd.
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Notes http://dx.doi.org/10.1111/gcb.12485
NOAA - No. NA10OAR4170060; No. NA08OAR4170669
istex:F2896505DB23C4CF91887263407ACF4070262F31
ArticleID:GCB12485
California Sea Grant College Program - No. R/CC-02EPD; No. R/CC-04; No. R/OPCENV-09
NSF-OCE - No. 0927445; No. 1041062
Data S1. Adult spawning and larval culturing.
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  year: 2014
  text: March 2014
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PublicationTitle Global change biology
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Publisher Blackwell Science
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Wiley-Blackwell
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References Lucas JS, Costlow JD (1979) Effects of various temperature cycles on the larval development of the gastropod mollusc Crepidula fornicata. Marine Biology, 51, 111-117.
Kurihara H, Asai T, Kato S, Ishimatsu A (2008) Effects of elevated pCO2 on early development in the mussel Mytilus galloprovincialis. Aquatic Biology, 4, 225-233.
Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science, 321, 926-929.
Clayton TD, Byrne RH (1993) Spectrophotometric seawater pH measurements: total hydrogen ion concentration scale calibration of m-cresol purple and at-sea results. Deep-Sea Research, 40, 2115-2129.
Dupont S, Lundve B, Thorndyke M (2010) Near future ocean acidification increases growth rate of the lecithotrophic larvae and juveniles of the sea star Crossaster papposus. Journal of Experimental Zoology, 314, 382-389.
Pörtner HO, Langenbuch M (2005) Synergistic effects of temperature extremes, hypoxia, and increases in CO2 on marine animals: from Earth history to global change. Journal of Geophysical Research, 110, C09S10.
Crawford WR, Peña MA (2013) Declining oxygen on the British Columbia continental shelf. Atmosphere-Ocean, 51, 88-103.
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. Geophysical Research Letters, 40, 2171-2176.
Rilov G, Dudas SE, Menge BA, Grantham BA, Lubchenco J, Schiel DR (2008) The surf zone: a semi-permeable barrier to onshore recruitment of invertebrate larvae? Journal of Experimental Marine Biology and Ecology, 361, 59-74.
Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Research, 34, 1733-1743.
Eerkes-Medrano D, Menge BA, Sislak C, Langdon CJ (2013) Contrasting effects of hypoxic conditions on survivorship of planktonic larvae of rocky intertidal invertebrates. Marine Ecology Progress Series, 478, 139-151.
Dufault AM, Cumbo VR, Fan T-Y, Edmunds PJ (2012) Effects of diurnally oscillating pCO2 on the calcification and survival of coral recruits. Proceedings of the Royal Society B, 279, 2951-2958.
Moran AL, Emlet RB (2001) Offspring size and performance in variable environments: field studies on a marine snail. Ecology, 82, 1597-1612.
Sastry AN (1979) Metabolic adaptation of Cancer irroratus developmental stages to cyclic temperatures. Marine Biology, 51, 243-250.
Hofmann GE, Smith JE, Johnson KS et al. (2011) High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS ONE, 6, e28983.
Shanks AL, Shearman RK (2009) Paradigm lost? Cross-shelf distributions of intertidal invertebrate larvae are unaffected by upwelling or downwelling. Marine Ecology Progress Series, 385, 189-204.
Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RN (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography, 18, 897-907.
Hayakaze E, Tanabe K (1999) Early larval shell development in mytilid bivalve Mytilus galloprovincialis. Venus, 58, 119-127.
Carson HS, López-Duarte PC, Rasmussen L, Wang D, Levin LA (2010) Reproductive timing alters population connectivity in marine metapopulations. Current Biology, 20, 1926-1931.
Orlando EF, Guillette LJ (2001) A re-examination of variaiton associated with environmentally stressed organisms. Human Reproduction Update, 7, 265-272.
Cai W-J, Hu X, Huang W-J et al. (2011) Acidification of subsurface coastal waters enhanced by eutrophication. Nature Geoscience, 4, 766-770.
Stramma L, Schmidtko S, Levin LA, Johnson GC (2010) Ocean oxygen minima expansions and their biological impacts. Deep-Sea Research, 57.4, 587-595.
Gobler CJ, Talmage SC (2013) Short- and long-term consequences of larval stage exposure to constantly and ephemerally elevated carbon dioxide for marine bivalve populations. Biogeosciences, 10, 2241-2253.
Feely RA, Sabine CL, Hernandez-Ayon JM, Ianson D, Hales B (2008) Evidence for upwelling of corrosive "acidified" water onto the continental shelf. Science, 320, 1490-1492.
Gaylord B, Hill TM, Sanford E et al. (2011) Functional impacts of ocean acidification in an ecologically critical foundation species. Journal of Experimental Biology, 214, 2586-2594.
Pechenik JA (1999) On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Marine Ecology Progress Series, 177, 269-297.
Hochachka PW, Somero GN (2002) Biochemical Adaptation: mechanism and Process in Physiological Evolution. Oxford University Press, New York.
Hauri C, Gruber N, Vogt M et al. (2013) Spatiotemporal variability and long-term trends of ocean acidification in the California Current System. Biogeosciences, 10, 193-216.
Kurihara H (2008) Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Marine Ecology Progress Series, 373, 275-284.
Dickson AG, Sabine CL, Christian JR (2007) Guide to Best Practices for Ocean CO2 Measurements. PICES Special Publication 3, Sidney, British Columbia.
Thomsen J, Gutowska MA, Saphörster J et al. (2010) Calcifying invertebrates succeed in a naturally CO2-rich coastal habitat but are threatened by high levels of future acidification. Biogeosciences, 7, 3879-3891.
White MM, McCorkle DC, Mullineaux LS, Cohen AL (2013) Early exposure of bay scallops (Argopecten irradians) to high CO2 causes a decrease in larval shell growth. PLoS ONE, 8, e61065.
Byrne M (2012) Global change ecotoxicology: Identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Marine Environmental Research, 76, 3-15.
Bates NR, Best MHP, Neely K, Garley R, Dickson AG, Johnson RJ (2012) Detecting anthropogenic carbon dioxide uptake and ocean acidification in the North Atlantic Ocean. Biogeosciences, 9, 2509-2522.
Bockmon EE, Frieder CA, Navarro MO, White-Kershek LA, Dickson AG (2013) Technical note: controlled experimental aquarium system for multi-stressor investigation of carbonate chemistry, oxygen saturation, and temperature. Biogeosciences, 10, 5967-5975.
Keeling RF, Körtzinger A, Gruber N (2010) Ocean deoxygenation in a warming world. Annual Review of Marine Science, 2, 199-229.
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.
Van Heuven SD, Pierrot JWB, Lewis RE, Wallace DWR (2011) MATLAB Program Developed for CO2 System Calculations, ORNL/CDIAC-105b. Oak Ridge, Tennessee, Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy.
Chan F, Barth JA, Lubchenco J, Kirincich A, Weeks H, Peterson WT, Menge BA (2008) Emergence of anoxia in the California current large marine ecosystem. Science, 319, 920.
Pörtner HO (2012) Integrating climate-related stressor effects on marine organisms: unifying principles linking molecule to ecosystem-level changes. Marine Ecology Progress Series, 470, 273-290.
Shanks AL, Brink L (2005) Upwelling, downwelling, and cross-shelf transport of bivalve larvae: test of a hypothesis. Marine Ecology Progress Series, 302, 1-12.
Gosselin LA, Chia F-S (1996) Prey selection by inexperienced predators: do early juvenile snails maximize net energy gains on their first attack? Journal of Experimental Marine Biology and Ecology, 199, 45-58.
Capone DG, Hutchins DA (2013) Microbial biogeochemistry of coastal upwelling regimes in a changing ocean. Nature Geoscience, 6, 711-717.
Bograd SJ, Castro CG, Di Lorenzo E, Palacios DM, Bailey H, Gilly W, Chavez FP (2008) Oxygen declines and the shoaling of the hypoxic boundary in the California Current. Geophysical Research Letters, 35, L12607.
Widdows J, Newell RIE, Mann R (1989) Effects of hypoxia and anoxia on survival, energy metabolism, and feeding of oyster larvae (Crassostrea virginica, Gmelin). Biological Bulletin, 177, 154-166.
Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. Proceedings of the National Academy of Sciences, 105, 15452-15457.
Wang W, Widdows J (1991) Physiological responses of mussel larvae Mytilus edulis to environmental hypoxia and anoxia. Marine Ecology Progress Series, 70, 223-236.
Hettinger A, Sanford E, Hill TM et al. (2012) Persistent carry-over effects of planktonic exposure to ocean acidification in the Olympia oyster. Ecology, 93, 2758-2768.
Wootton JT, Pfister CA, Forester JD (2008) Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. Proceedings of the National Academy of Sciences, 105, 18848-18853.
Wilt FH (2005) Development biology meets material science: morphogenesis of biomineralized structures. Developmental Biology, 280, 15-25.
Booth JAT, McPhee-Shaw EE, Chua P et al. (2012) Natural intrusions of hypoxic, low pH water into nearshore marine environments on the California coast. Continental Shelf Research, 45, 108-115.
Gazeau F, Gattuso J-P, Greaves M, Elderfield H, Peene J, Heip CHR, Middelburg JJ (2011) Effect of carbonate chemistry alteration on the early embryonic development of the Pacific oyster (Crassostrea gigas). PLoS ONE, 6, e23010.
Whitney FA, Freeland HJ, Robert M (2007) Persistently declining oxygen levels in the interior waters of the eastern subarctic Pacific. Progress in Oceanography, 75, 179-199.
1987; 34
1976
1973; 18
2008; 35
2008; 105
1971
2008; 4
2007; 75
2013; 8
2013; 6
2010; 20
2013; 10
2010; 314
2013; 51
2013; 478
2005; 302
2008; 319
1999; 58
2010; 57.4
1999; 177
2010; 2
2010; 7
2011; 214
1993; 40
2005; 110
2011
2013; 40
1989; 177
2007
1995
2002
2011; 4
2008; 321
2008; 320
2011; 6
2012; 76
2008; 361
1979; 51
2012; 93
2012; 470
2001; 82
2005; 280
2001; 7
2009; 385
1991; 70
1996; 199
2013
2012; 279
2012; 45
2008; 373
2012; 9
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References_xml – reference: Hauri C, Gruber N, Vogt M et al. (2013) Spatiotemporal variability and long-term trends of ocean acidification in the California Current System. Biogeosciences, 10, 193-216.
– reference: Sastry AN (1979) Metabolic adaptation of Cancer irroratus developmental stages to cyclic temperatures. Marine Biology, 51, 243-250.
– reference: Thomsen J, Gutowska MA, Saphörster J et al. (2010) Calcifying invertebrates succeed in a naturally CO2-rich coastal habitat but are threatened by high levels of future acidification. Biogeosciences, 7, 3879-3891.
– reference: Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Research, 34, 1733-1743.
– reference: Hochachka PW, Somero GN (2002) Biochemical Adaptation: mechanism and Process in Physiological Evolution. Oxford University Press, New York.
– reference: Lucas JS, Costlow JD (1979) Effects of various temperature cycles on the larval development of the gastropod mollusc Crepidula fornicata. Marine Biology, 51, 111-117.
– reference: Byrne M (2012) Global change ecotoxicology: Identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches. Marine Environmental Research, 76, 3-15.
– reference: Capone DG, Hutchins DA (2013) Microbial biogeochemistry of coastal upwelling regimes in a changing ocean. Nature Geoscience, 6, 711-717.
– reference: Gazeau F, Gattuso J-P, Greaves M, Elderfield H, Peene J, Heip CHR, Middelburg JJ (2011) Effect of carbonate chemistry alteration on the early embryonic development of the Pacific oyster (Crassostrea gigas). PLoS ONE, 6, e23010.
– reference: Chan F, Barth JA, Lubchenco J, Kirincich A, Weeks H, Peterson WT, Menge BA (2008) Emergence of anoxia in the California current large marine ecosystem. Science, 319, 920.
– reference: Hayakaze E, Tanabe K (1999) Early larval shell development in mytilid bivalve Mytilus galloprovincialis. Venus, 58, 119-127.
– reference: Bates NR, Best MHP, Neely K, Garley R, Dickson AG, Johnson RJ (2012) Detecting anthropogenic carbon dioxide uptake and ocean acidification in the North Atlantic Ocean. Biogeosciences, 9, 2509-2522.
– reference: Shanks AL, Brink L (2005) Upwelling, downwelling, and cross-shelf transport of bivalve larvae: test of a hypothesis. Marine Ecology Progress Series, 302, 1-12.
– reference: Gobler CJ, Talmage SC (2013) Short- and long-term consequences of larval stage exposure to constantly and ephemerally elevated carbon dioxide for marine bivalve populations. Biogeosciences, 10, 2241-2253.
– reference: 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. Geophysical Research Letters, 40, 2171-2176.
– reference: Moran AL, Emlet RB (2001) Offspring size and performance in variable environments: field studies on a marine snail. Ecology, 82, 1597-1612.
– reference: Dupont S, Lundve B, Thorndyke M (2010) Near future ocean acidification increases growth rate of the lecithotrophic larvae and juveniles of the sea star Crossaster papposus. Journal of Experimental Zoology, 314, 382-389.
– reference: Dufault AM, Cumbo VR, Fan T-Y, Edmunds PJ (2012) Effects of diurnally oscillating pCO2 on the calcification and survival of coral recruits. Proceedings of the Royal Society B, 279, 2951-2958.
– reference: Hettinger A, Sanford E, Hill TM et al. (2012) Persistent carry-over effects of planktonic exposure to ocean acidification in the Olympia oyster. Ecology, 93, 2758-2768.
– reference: Cai W-J, Hu X, Huang W-J et al. (2011) Acidification of subsurface coastal waters enhanced by eutrophication. Nature Geoscience, 4, 766-770.
– reference: Hofmann GE, Smith JE, Johnson KS et al. (2011) High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS ONE, 6, e28983.
– reference: Orlando EF, Guillette LJ (2001) A re-examination of variaiton associated with environmentally stressed organisms. Human Reproduction Update, 7, 265-272.
– reference: Shanks AL, Shearman RK (2009) Paradigm lost? Cross-shelf distributions of intertidal invertebrate larvae are unaffected by upwelling or downwelling. Marine Ecology Progress Series, 385, 189-204.
– reference: Wang W, Widdows J (1991) Physiological responses of mussel larvae Mytilus edulis to environmental hypoxia and anoxia. Marine Ecology Progress Series, 70, 223-236.
– reference: Dickson AG, Sabine CL, Christian JR (2007) Guide to Best Practices for Ocean CO2 Measurements. PICES Special Publication 3, Sidney, British Columbia.
– reference: Pörtner HO (2012) Integrating climate-related stressor effects on marine organisms: unifying principles linking molecule to ecosystem-level changes. Marine Ecology Progress Series, 470, 273-290.
– reference: Van Heuven SD, Pierrot JWB, Lewis RE, Wallace DWR (2011) MATLAB Program Developed for CO2 System Calculations, ORNL/CDIAC-105b. Oak Ridge, Tennessee, Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy.
– reference: Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. Proceedings of the National Academy of Sciences, 105, 15452-15457.
– reference: Gaylord B, Hill TM, Sanford E et al. (2011) Functional impacts of ocean acidification in an ecologically critical foundation species. Journal of Experimental Biology, 214, 2586-2594.
– reference: Feely RA, Sabine CL, Hernandez-Ayon JM, Ianson D, Hales B (2008) Evidence for upwelling of corrosive "acidified" water onto the continental shelf. Science, 320, 1490-1492.
– reference: Widdows J, Newell RIE, Mann R (1989) Effects of hypoxia and anoxia on survival, energy metabolism, and feeding of oyster larvae (Crassostrea virginica, Gmelin). Biological Bulletin, 177, 154-166.
– reference: Bockmon EE, Frieder CA, Navarro MO, White-Kershek LA, Dickson AG (2013) Technical note: controlled experimental aquarium system for multi-stressor investigation of carbonate chemistry, oxygen saturation, and temperature. Biogeosciences, 10, 5967-5975.
– reference: Eerkes-Medrano D, Menge BA, Sislak C, Langdon CJ (2013) Contrasting effects of hypoxic conditions on survivorship of planktonic larvae of rocky intertidal invertebrates. Marine Ecology Progress Series, 478, 139-151.
– reference: Rilov G, Dudas SE, Menge BA, Grantham BA, Lubchenco J, Schiel DR (2008) The surf zone: a semi-permeable barrier to onshore recruitment of invertebrate larvae? Journal of Experimental Marine Biology and Ecology, 361, 59-74.
– reference: Gosselin LA, Chia F-S (1996) Prey selection by inexperienced predators: do early juvenile snails maximize net energy gains on their first attack? Journal of Experimental Marine Biology and Ecology, 199, 45-58.
– reference: White MM, McCorkle DC, Mullineaux LS, Cohen AL (2013) Early exposure of bay scallops (Argopecten irradians) to high CO2 causes a decrease in larval shell growth. PLoS ONE, 8, e61065.
– reference: Wilt FH (2005) Development biology meets material science: morphogenesis of biomineralized structures. Developmental Biology, 280, 15-25.
– reference: Wootton JT, Pfister CA, Forester JD (2008) Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. Proceedings of the National Academy of Sciences, 105, 18848-18853.
– reference: Keeling RF, Körtzinger A, Gruber N (2010) Ocean deoxygenation in a warming world. Annual Review of Marine Science, 2, 199-229.
– reference: Pechenik JA (1999) On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Marine Ecology Progress Series, 177, 269-297.
– reference: Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RN (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography, 18, 897-907.
– reference: Booth JAT, McPhee-Shaw EE, Chua P et al. (2012) Natural intrusions of hypoxic, low pH water into nearshore marine environments on the California coast. Continental Shelf Research, 45, 108-115.
– reference: Whitney FA, Freeland HJ, Robert M (2007) Persistently declining oxygen levels in the interior waters of the eastern subarctic Pacific. Progress in Oceanography, 75, 179-199.
– reference: Kurihara H (2008) Effects of CO2-driven ocean acidification on the early developmental stages of invertebrates. Marine Ecology Progress Series, 373, 275-284.
– reference: Kurihara H, Asai T, Kato S, Ishimatsu A (2008) Effects of elevated pCO2 on early development in the mussel Mytilus galloprovincialis. Aquatic Biology, 4, 225-233.
– reference: Carson HS, López-Duarte PC, Rasmussen L, Wang D, Levin LA (2010) Reproductive timing alters population connectivity in marine metapopulations. Current Biology, 20, 1926-1931.
– reference: Crawford WR, Peña MA (2013) Declining oxygen on the British Columbia continental shelf. Atmosphere-Ocean, 51, 88-103.
– reference: Bograd SJ, Castro CG, Di Lorenzo E, Palacios DM, Bailey H, Gilly W, Chavez FP (2008) Oxygen declines and the shoaling of the hypoxic boundary in the California Current. Geophysical Research Letters, 35, L12607.
– reference: Clayton TD, Byrne RH (1993) Spectrophotometric seawater pH measurements: total hydrogen ion concentration scale calibration of m-cresol purple and at-sea results. Deep-Sea Research, 40, 2115-2129.
– reference: Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science, 321, 926-929.
– reference: 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.
– reference: Pörtner HO, Langenbuch M (2005) Synergistic effects of temperature extremes, hypoxia, and increases in CO2 on marine animals: from Earth history to global change. Journal of Geophysical Research, 110, C09S10.
– reference: Stramma L, Schmidtko S, Levin LA, Johnson GC (2010) Ocean oxygen minima expansions and their biological impacts. Deep-Sea Research, 57.4, 587-595.
– year: 2011
– volume: 40
  start-page: 2115
  year: 1993
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Snippet Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O₂]) levels. In...
Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O2]) levels. In...
Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O 2 ]) levels. In...
Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O2 ]) levels. In...
Natural variation and changing climate in coastal oceans subject meroplanktonic organisms to broad ranges of pH and oxygen ([O sub(2)]) levels. In...
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SubjectTerms Acidification
Animal and plant ecology
Animal, plant and microbial ecology
Animals
Biological and medical sciences
chemistry
climate
Climate change
coastal variability
Diurnal variations
Fluctuations
Fundamental and applied biological sciences. Psychology
General aspects
growth & development
Hydrogen-Ion Concentration
Invertebrates
Larva
Larva - growth & development
Larva - metabolism
Larvae
Larval development
Marine
Marine biology
metabolism
Mollusca
Mollusks
multistressor
mussel
mussels
Mytilus
Mytilus - growth & development
Mytilus - metabolism
Mytilus californianus
Ocean acidification
Oceans
Oceans and Seas
oxygen
Oxygen - metabolism
planktonic larvae
Seawater
Seawater - chemistry
semidiurnal pH fluctuations
survival rate
variance
Title Can variable pH and low oxygen moderate ocean acidification outcomes for mussel larvae?
URI https://api.istex.fr/ark:/67375/WNG-ZFB9BQC3-J/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fgcb.12485
https://www.ncbi.nlm.nih.gov/pubmed/24343909
https://www.proquest.com/docview/1491993543
https://www.proquest.com/docview/1492723415
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Volume 20
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