Interactive effects of acidification, hypoxia, and thermal stress on growth, respiration, and survival of four North Atlantic bivalves
Open accessAbstract
We investigated the individual and interactive effects of coastal and climate change stressors (elevated temperatures, acidification, and hypoxia) on the growth, survival, and respiration rates of 4 commercially and ecologically important North Atlantic bivalves: bay scallops Argopecten irradians, Eastern oysters Crassostrea virginica, blue mussels Mytilus edulis, and hard clams Mercenaria mercenaria.Month-long experiments were performed on multiple cohorts of post-set juveniles using conditions commonly found during summer months within eutrophied, shallow, temperate, coastal environments (24-31°C; 2-7 mg O 2 l -1 ; pH T , total scale, 7.2-8.0).Elevated temperatures most consistently altered the performance of the bivalves, with both positive and negative physiological consequences.Low levels of dissolved oxygen (DO) and pH individually reduced the survival, shell growth, and/or tissue weight of each bivalve, with A. irradians being the most vulnerable species.Low DO also significantly increased respiration rates of A. irradians and M. mercenaria, evidencing a compensatory physiological response to hypoxia.M. edulis and M. mercenaria both displayed size-dependent vulnerability to acidification, with smaller individuals being more susceptible.The combination of low DO and low pH often interacted antagonistically to yield growth rates higher than would be predicted from either individual stressor, potentially suggesting that some anaerobic metabolic pathways may function optimally under hypercapnia.Elevated temperature and low pH interacted both antagonistically and synergistically, producing outcomes that could not be predicted from the responses to individual stressors.Collectively, this study revealed species-and size-specific vulnerabilities of bivalves to coastal stressors along with unpredicted interactions among those stressors. KEY WORDS: Bay scallops •
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Bay scallops are considered among the more sensitive of the regional bivalve fishery species to global change stressors.
“as bay scallops are considered among the more sensitive of the regional bivalve fishery species to global change stressors (Grear et al., 2020;Stevens & Gobler, 2018).”
From Warming and hypoxia reduce the performance and survival of northern bay scallops (<i>Argopecten irradians irradians</i>) amid a fishery collapse (2023) · cites this paper as Stevens & Gobler, 2018
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Spreading dead zones and consequences for marine ecosystems
Diaz, R. J., & Rosenberg, R. (2008) · Science · doi:10.1126/science.1156401 · Cited by 6,626 · see citing works
Coral Reefs Under Rapid Climate Change and Ocean Acidification
Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfield, P., Gomez, E., Harvell, C. D., Sale, P. F., Edwards, A. J., Caldeira, K., et al. (2007) · Science · doi:10.1126/science.1152509 · Cited by 5,885 · see citing works
Ocean Deoxygenation in a Warming World
Keeling, R. F., Körtzinger, A., & Gruber, N. (2010) · Annual Review of Marine Science · doi:10.1146/annurev.marine.010908.163855 · Cited by 1,712 · see citing works
Coastal ocean acidification: The other eutrophication problem
Wallace, R. B., Baumann, H., Grear, J. S., Aller, R. C., & Gobler, C. J. (2014) · Estuarine, Coastal and Shelf Science · doi:10.1016/j.ecss.2014.05.027 · Cited by 607 · see citing works
Self-citationWarming up, turning sour, losing breath: ocean biogeochemistry under global change
Gruber, N. (2011) · Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences · doi:10.1098/rsta.2011.0003 · Cited by 588 · see citing works
Talmage, S. C., & Gobler, C. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0913804107 · Cited by 381 · see citing works
Self-citationGobler, C. J., DePasquale, E. L., Griffith, A. W., & Baumann, H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0083648 · Cited by 260 · see citing works
Self-citationGobler, C. J., Lonsdale, D. J., & Boyer, G. L. (2005) · Estuaries · doi:10.1007/bf02732911 · Cited by 176 · see citing works
Self-citationSize-dependent pH effect on calcification in post-larval hard clam Mercenaria spp
Waldbusser, G., Bergschneider, H., & Green, M. (2010) · Marine Ecology Progress Series · doi:10.3354/meps08809 · Cited by 127 · see citing works
Cardiac responses of the bay scallop Argopecten irradians to diel-cycling hypoxia
Gurr, S. J., Goleski, J., Lima, F. P., Seabra, R., Gobler, C. J., & Volkenborn, N. (2018) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2017.12.011 · Cited by 32 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 68
- Berge JA, Bjerkeng B, Pettersen O, Schaanning MT, Sigurd Øxnevad S (2006) Effects of increased sea water concen- trations of CO 2 on growth of the bivalve Mytilus edulis L. Chemosphere 62: 681-687 · DOI
- Boyd PW, Lennartz ST, Glover DM, Doney SC (2015) Biolog- ical ramifications of climate-change-mediated oceanic multi-stressors. Nat Clim Chang 5: 71-79 · DOI
- Breitburg D (2002) Effects of hypoxia, and the balance between hypoxia and enrichment, on coastal fishes and fisheries. Estuaries 25: 767-781 · DOI · Paper page
- Breitburg DL, Adamack A, Rose KA, Kolesar SE and others (2003) The pattern and influence of low dissolved oxygen in the Patuxent River, a seasonally hypoxic estuary. Estu- aries 26: 280-297 · DOI
- Breitburg DL, Hondorp DW, Davias LA, Diaz RJ (2009) Hypoxia, nitrogen, and fisheries: integrating effects across local and global landscapes. Annu Rev Mar Sci 1: 329-349 · DOI
- Cai WJ, Hu X, Huang WJ, Murrell MC and others (2011) Acidification of subsurface coastal waters enhanced by eutrophication. Nat Geosci 4: 766-770 · DOI · Paper page
- Cai WJ, Huang WJ, Luther GW III, Pierrot D and others (2017) Redox reactions and weak buffering capacity lead to acidification in the Chesapeake Bay. Nat Comm 8: 369 · DOI
- Carroll J, Gobler CJ, Peterson BJ (2008) Resource-restricted growth of eelgrass in New York estuaries: light limita- tion, and alleviation of nutrient stress by hard clams. Mar Ecol Prog Ser 369: 51-62 · DOI
- Cerrato RM, Caron DA, Lonsdale DJ, Rose JM, Schaffner RA (2004) Effect of the northern quahog Mercenaria mercenaria on the development of blooms of the brown tide alga Aureococcus anophagefferens. Mar Ecol Prog Ser 281: 93-108 · DOI
- Clark HR, Gobler CJ (2016) Diurnal fluctuations in CO 2 and dissolved oxygen concentrations do not provide a refuge from hypoxia and acidification for early-life-stage bivalves. Mar Ecol Prog Ser 558: 1-14 · DOI
- Cooley SR, Doney SC (2009) Anticipating ocean acidifica- tion's economic consequences for commercial fisheries. Environ Res Lett 4: 024007 · DOI
- Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11: 1304-1315 · DOI · Paper page
- Dame RF (1996) Ecology of marine bivalves: an ecosystem approach. CRC Press, New York, NY
- DeFur PL, Mangum CP (1979) The effect of environmental variables on the heart rates of invertebrates. Comp Biochem Physiol A Physiol 62: 283-294 · DOI
- Deutsch C, Ferrel A, Seibel B, Pörtner HO, Huey RB (2015) Climate change tightens a metabolic constraint on mar- ine habitats. Science 348: 1132-1135 · DOI · Paper page
- Diaz RJ, Rosenberg R (1995) Marine benthic hypoxia: a review of its ecological effects and the behavioural re - sponses of benthic macrofauna. Oceanogr Mar Biol Annu Rev 33: 245-303
- Dickson AG (1993) pH buffers for sea-water media based on the total hydrogen-ion concentration scale. Deep Sea Res I 40: 107-118 · DOI · Paper page
- Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO 2 problem. Annu Rev Mar Sci 1: 169-192 · DOI · Paper page
- Doney SC, Ruckelshaus M, Duffy JE, Barry JP and others (2012) Climate change impacts on marine ecosystems. Annu Rev Mar Sci 4: 11-37 · DOI · Paper page
- Ekstrom JA, Suatoni L, Cooley SR, Pendleton LH and others (2015) Vulnerability and adaptation of US shellfisheries to ocean acidification. Nat Clim Chang 5: 207-214 · DOI
- Feely RA, Alin SR, Newton J, Sabine CL and others (2010) The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urban- ized estuary. Estuar Coast Shelf Sci 88: 442-449 · DOI
- Gazeau F, Parker LM, Comeau S, Gattuso JP and others (2013) Impacts of ocean acidification on marine shelled molluscs. Mar Biol 160: 2207-2245 · DOI
- Gledhill DK, White MM, Salisbury J, Thomas H and others (2015) Ocean and coastal acidification off New England and Nova Scotia. Oceanography 28: 182-197 · DOI
- Gobler CJ, Baumann H (2016) Hypoxia and acidification in ocean ecosystems: coupled dynamics and effects on marine life. Biol Lett 12: 20150976 · DOI · Paper page
- Gobler CJ, Talmage SC (2013) Short-and long-term conse- quences of larval stage exposure to constantly and ephemerally elevated carbon dioxide for marine bivalve populations. Biogeosciences 10: 2241-2253 · DOI · Paper page
- Gobler CJ, Talmage SC (2014) Physiological response and resilience of early life-stage Eastern oysters (Crassostrea virginica) to past, present and future ocean acidification. Conserv Physiol 2: cou004 · DOI
- Green MA, Waldbusser GG, Reilly SL, Emerson K, O'Don- nell S (2009) Death by dissolution: sediment saturation state as a mortality factor for juvenile bivalves. Limnol Oceanogr 54: 1037-1047 · DOI · Paper page
- Grieshaber MK, Hardewig I, Kreutzer U, Pörtner HO (1994) Physiological and metabolic responses to hypoxia in in - vertebrates. Rev Physiol Biochem Pharmacol 125: 43-147 · DOI · Paper page
- Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generaliza- tions. Biol Rev Camb Philos Soc 74: 1-40 · DOI
- Hamwi A, Haskin HH (1969) Oxygen consumption and pumping rates in the hard clam Mercenaria mercenaria: a direct method. Science 163: 823-824 · DOI
- Hochachka PW, Lutz PL (2001) Mechanism, origin, and evo- lution of anoxia tolerance in animals. Comp Biochem Physiol B Biochem Mol Biol 130: 435-459 · DOI · Paper page
- Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world's marine ecosystems. Science 328: 1523-1528 · DOI
- Jansson A, Norkko J, Dupont S, Norkko A (2015) Growth and survival in a changing environment: combined effects of moderate hypoxia and low pH on juvenile bivalve Macoma balthica. J Sea Res 102: 41-47 · DOI
- Kennedy VS, Newell RIE, Eble AF (1996) The eastern oyster: Crassostrea virginica. Maryland Sea Grant College, Col- lege Park, MD Kraeuter JN, Castagna M (2001) Biology of the hard clam. Elsevier Science, New York, NY
- Levin LA, Ekau W, Gooday AJ, Jorissen F and others (2009) Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences 6: 2063-2098 · DOI
- Lüthi D, Le Floch M, Bereiter B, Blunier T and others (2008) High-resolution carbon dioxide concentration record 650, 000-800, 000 years before present. Nature 453: 379-382 · DOI
- Martínez ML, Intralawan A, Vázquez G, Pérez-Maqueo O, Sutton P, Landgrave R (2007) The coasts of our world: ecological, economic and social importance. Ecol Econ 63: 254-272 · DOI
- Melzner F, Thomsen J, Koeve W, Oschlies A and others (2013) Future ocean acidification will be amplified by hypoxia in coastal habitats. Mar Biol 160: 1875-1888 · DOI · Paper page
- Millero FJ (2010) Carbonate constants for estuarine waters. Mar Freshw Res 61: 139-142 · DOI
- Newell RI (2004) Ecosystem influences of natural and culti- vated populations of suspension-feeding bivalve mol- luscs: a review. J Shellfish Res 23: 51-62
- Nixon SW (1995) Coastal marine eutrophication: a defini- tion, social causes, and future concerns. Ophelia 41: 199-219 · DOI
- Nixon SW, Granger S, Buckley BA, Lamont M, Rowell B (2004) A one hundred and seventeen year coastal water temperature record from Woods Hole, Massachusetts. Estuaries 27: 397-404 · DOI
- Officer CB, Smayda TJ, Mann R (1982) Benthic filter feed- ing: a natural eutrophication control. Mar Ecol Prog Ser 9: 203-210 · DOI
- Pörtner HO (2008) Ecosystem effects of ocean acidification in times of ocean warming: a physiologist's view. Mar Ecol Prog Ser 373: 203-217 · DOI
- Pörtner HO (2010) Oxygen-and capacity-limitation of ther- mal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213: 881-893 · DOI · Paper page
- Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322: 690-692 · DOI · Paper page
- Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal toler- ance. Science 315: 95-97 · DOI · Paper page
- Pörtner HO, Langenbuch M, Michaelidis B (2005) Synergis- tic effects of temperature extremes, hypoxia, and in - creases in CO 2 on marine animals: from Earth history to global change. J Geophys Res Oceans 110:C09S10 · DOI
- Rabalais NN, Diaz RJ, Levin LA, Turner RE, Gilbert D, Zhang J (2010) Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences 7: 585-619 · DOI
- Range P, Chícharo MA, Ben-Hamadou R, Piló D, Fernandez- Reiriz MJ, Labarta U, Munari M (2014) Impacts of CO 2 - induced seawater acidification on coastal Mediterranean bivalves and interactions with other climatic stressors. Reg Environ Change 14: 19-30 · DOI
- Reynaud S, Leclercq N, Romaine Lioud S, Ferrier Pagés C, Jaubert J, Gattuso JP (2003) Interacting effects of CO 2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Glob Change Biol 9: 1660-1668 · DOI
- Shumway SE, Parsons GJ (2006) Scallops: biology, ecology, and aquaculture. Elsevier, Boston, MA
- Sokolova IM (2013) Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integr Comp Biol 53: 597-608 · DOI · Paper page
- Stickle WB, Kapper MA, Liu LL, Gnaiger E, Wang SY (1989) Metabolic adaptations of several species of crustaceans and molluscs to hypoxia: tolerance and microcalorimetric studies. Biol Bull (Woods Hole) 177: 303-312 · DOI
- Sui Y, Kong H, Shang Y, Huang X, Wu F, Hu M, Wang Y (2016) Effects of short-term hypoxia and seawater acidi- fication on hemocyte responses of the mussel Mytilus coruscus. Mar Pollut Bull 108: 46-52 · DOI
- Sunday JM, Bates AE, Dulvy NK (2012) Thermal tolerance and the global redistribution of animals. Nat Clim Chang 2: 686-690 · DOI · Paper page
- Talmage SC, Gobler CJ (2009) The effects of elevated car- bon dioxide concentrations on the metamorphosis, size, and survival of larval hard clams (Mercenaria merce- naria), bay scallops (Argopecten irradians), and Eastern oysters (Crassostrea virginica). Limnol Oceanogr 54: 2072-2080 · DOI · Paper page
- Talmage SC, Gobler CJ (2011) Effects of elevated tempera- ture and carbon dioxide on the growth and survival of larvae and juveniles of three species of Northwest Atlantic bivalves. PLOS ONE 6: e26941 · DOI
- Thomsen J, Melzner F (2010) Moderate seawater acidifica- tion does not elicit long-term metabolic depression in the blue mussel Mytilus edulis. Mar Biol 157: 2667-2676 · DOI
- Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. Proc Natl Acad Sci USA 105: 15452-15457 · DOI · Paper page
- 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 sen- sitivity. Geophys Res Lett 40: 2171-2176 · DOI
- Waldbusser GG, Hales B, Langdon CJ, Haley BA and others (2015) Ocean acidification has multiple modes of action on bivalve larvae. PLOS ONE 10: e0128376 · DOI
- Waldbusser GG, Gray MW, Hales B, Langdon CJ and others (2016) Slow shell building, a possible trait for resistance to the effects of acute ocean acidification. Limnol Oceanogr 61: 1969-1983 · DOI
- Wall CC, Peterson BJ, Gobler CJ (2008) Facilitation of sea- grass Zostera marina productivity by suspension-feeding bivalves. Mar Ecol Prog Ser 357: 165-174 · DOI
- Wang K, Espinosa EP, Allam B (2016) Effect of 'heat shock' treatments on QPX disease and stress response in the hard clam, Mercenaria mercenaria. J Invertebr Pathol 138: 39-49 · DOI
- Weiss MB, Curran PB, Peterson BJ, Gobler CJ (2007) The influence of plankton composition and water quality on hard clam (Mercenaria mercenaria L.) populations across Long Island's south shore lagoon estuaries (New York, USA). J Exp Mar Biol Ecol 345: 12-25 · DOI
- Wu RSS (2002) Hypoxia: from molecular responses to eco- system responses. Mar Pollut Bull 45: 35-45 · DOI
- Zhang J, Gilbert D, Gooday AJ, Levin L and others (2010) Natural and human-induced hypoxia and consequences for coastal areas: synthesis and future development. Bio- geosciences 7: 1443-1467 Editorial responsibility: Emily Carrington, Friday Harbor, Washington, USA Submitted: October 29, 2017; Accepted: August 15, 2018 Proofs received from author(s): September 21, 2018 · DOI
Cited by
Sorted by citations
Tomasetti, S. J., Hallinan, B. D., Tettelbach, S. T., Volkenborn, N., Doherty, O. W., Allam, B., & Gobler, C. J. (2023) · Global Change Biology · doi:10.1111/gcb.16575 · Cited by 58 · see citing works
“…bivalve populations will be susceptible to the combination of warming and hypoxia under continued climate change is unknown, as bay scallops are considered among the more sensitive of the regional bivalve fishery species to global change stressors (Grear et al., 2020; Stevens & Gobler, 2018).”
BackgroundInfluentialSelf-citation
- Authors
- Stevens, A., & Gobler, C.
- Affiliations
- Stony Brook University (US)
- Corresponding author
- Gobler, CJ
- Venue
- Marine Ecology Progress Series
- Publisher
- Inter-Research Science Center
- Published
- 2018-10-04
- Volume
- 604
- Pages
- 143-161
- ISSN
- 0171-8630 (ISSN-L)
- 1616-1599
- OpenAlex
- W2889480565
- Cited by
- 112
- References
- 10
- Citations by year
- 2026: 14 · 2025: 20 · 2024: 14 · 2023: 25 · 2022: 14 · 2021: 11 · 2020: 9 · 2019: 4 · 2018: 1
- FWCI
- 4.02
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Marine Ecology Progress Series (publishedVersion)
- Funders
- Simons Foundation
- Chicago Community Trust
- Laurie Landeau Foundation
- New York Sea Grant, State University of New York (R-FBM-38)
- Topics
- Physical Sciences › Earth and Planetary Sciences › Oceanography › Ocean Acidification Effects and Responses
- Physical Sciences › Environmental Science › Global and Planetary Change › Marine Bivalve and Aquaculture Studies
- Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
- Keywords
- ocean acidification, hypoxia, thermal stress (biology), bivalve physiology, Argopecten irradians, Crassostrea virginica, Mytilus edulis, Mercenaria mercenaria, shell growth, respiration rate, survival, stressor interactions, eutrophication, climate change
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review