Multistressor impacts of warming and acidification of the ocean on marine invertebrates’ life histories

Byrne, M.; Przeslawski, R.

doi:10.1093/icb/ict049

Cited by 388Ocean Acidification Effects and ResponsesCoral and Marine Ecosystems StudiesPhysiological and biochemical adaptations

Multistressor impacts of warming and acidification of the ocean on marine invertebrates’ life histories

Byrne, M., Przeslawski, R.·2013·Integrative and Comparative Biology

DOI 10.1093/icb/ict049

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Abstract

Benthic marine invertebrates live in a multistressor world where stressor levels are, and will continue to be, exacerbated by global warming and increased atmospheric carbon dioxide. These changes are causing the oceans to warm, decrease in pH, become hypercapnic, and to become less saturated in carbonate minerals. These stressors have strong impacts on biological processes, but little is known about their combined effects on the development of marine invertebrates. Increasing temperature has a stimulatory effect on development, whereas hypercapnia can depress developmental processes. The pH, pCO2, and CaCO3 of seawater change simultaneously with temperature, challenging our ability to predict future outcomes for marine biota. The need to consider both warming and acidification is reflected in the recent increase in cross-factorial studies of the effects of these stressors on development of marine invertebrates. The outcomes and trends in these studies are synthesized here. Based on this compilation, significant additive or antagonistic effects of warming and acidification of the ocean are common (16 of 20 species studied), and synergistic negative effects also are reported. Fertilization can be robust to near-future warming and acidification, depending on the male-female mating pair. Although larvae and juveniles of some species tolerate near-future levels of warming and acidification (+2°C/pH 7.8), projected far-future conditions (ca. ≥4°C/ ≤pH 7.6) are widely deleterious, with a reduction in the size and survival of larvae. It appears that larvae that calcify are sensitive both to warming and acidification, whereas those that do not calcify are more sensitive to warming. Different sensitivities of life-history stages and species have implications for persistence and community function in a changing ocean. Some species are more resilient than others and may be potential "winners" in the climate-change stakes. As the ocean will change more gradually over coming decades than in "future shock" perturbation investigations, it is likely that some species, particularly those with short generation times, may be able to tolerate near-future oceanic change through acclimatization and/or adaption.

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Interactive effects of multiple stressors are often manifested in a species-, strain-, and stressor-specific manner and are the outcome of complex biotic and abiotic processes.
“Interactive effects are often manifested in a species-, strain-, and stressor-specific manner and are the outcome of complex biotic and abiotic processes (Crain et al., 2008;Melzner et al., 2011Melzner et al., , 2011;;Byrne and Przeslawski, 2013;Griffith and Gobler, 2016).”
From Harmful algal blooms: A climate change co-stressor in marine and freshwater ecosystems (2020) · cites this paper as Byrne and Przeslawski, 2013
The combined occurrences of two or more climate change stressors can often have even more complex and intense negative outcomes than individual stressors.
“The combined occurrences of two or more stressors can often have even more complex and intense negative outcomes (Melzner et al., 2011;Byrne and Przeslawski, 2013;Gobler et al., 2014).”
From Harmful algal blooms: A climate change co-stressor in marine and freshwater ecosystems (2020) · cites this paper as Byrne and Przeslawski, 2013

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Albright, R., Bland, C., Gillette, P. R., Serafy, J. E., Langdon, C., & Capo, T. R. (2012) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2012.05.017 · Cited by 55 · see citing works
High CO2 reduces the settlement of a spawning coral on three common species of crustose coralline algae
Doropoulos, C., & Díaz-Pulido, G. (2012) · Marine Ecology Progress Series · doi:10.3354/meps10096 · Cited by 53 · see citing works
Ocean acidification and warming reduce juvenile survival of the fluted giant clam, Tridacna squamosa
Watson, S., Southgate, P. C., Miller, G. M., MOORHEAD, J. A., & Knauer, J. (2012) · Molluscan Research · doi:10.11646/mr.32.3.7 · Cited by 53 · see citing works
Effects of temperature on hatching rate, embryonic development and early larval survival of the edible sea urchin, Tripneustes gratilla
Rahman, S. M., Tsuchiya, M., & Uehara, T. (2009) · Biologia · doi:10.2478/s11756-009-0135-2 · Cited by 53 · see citing works
Complex Responses of Intertidal Molluscan Embryos to a Warming and Acidifying Ocean in the Presence of UV Radiation
Davis, A. R., Coleman, D. W., Broad, A., Byrne, M., Dworjanyn, S. A., & Przeslawski, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055939 · Cited by 51 · see citing works
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Impact of climate change stressors on marine invertebrate life histories with a focus on the Mollusca and Echinodermata
Byrne, M. (2010) · Sydney University Press eBooks · doi:10.2307/j.ctv2kg15wg.10 · Cited by 51 · see citing works
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Impacts of temperature and acidification on larval calcium incorporation of the spider crab Hyas araneus from different latitudes (54° vs. 79°N)
Walther, K., Sartoris, F.-J., & Pörtner, H. (2011) · Marine Biology · doi:10.1007/s00227-011-1711-x · Cited by 45 · see citing works
Temperature and the Larval Ecology of the Crown-of-Thorns Starfish, Acanthaster planci
Johnson, L. G., & Babcock, R. C. (1994) · Biological Bulletin · doi:10.2307/1542287 · Cited by 45 · see citing works
Effects of high temperature on larval development and metamorphosis of Arachnoides placenta (Echinodermata: Echinoidea)
Chen, C. P., & Chen, B. Y. (1992) · Marine Biology · doi:10.1007/bf00356290 · Cited by 44 · see citing works
Climate change reduces offspring fitness in littoral spawners: a study integrating organismic response and long‐term time‐series
Bartolini, F., Barausse, A., Pörtner, H., & Giomi, F. (2012) · Global Change Biology · doi:10.1111/gcb.12050 · Cited by 41 · see citing works
Cellular responses of encapsulated gastropod embryos to multiple stressors associated with climate change
Deschaseaux, E. S. M., Taylor, A. M., Maher, W. A., & Davis, A. R. (2010) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2009.12.013 · Cited by 35 · see citing works
Temperature effects on periodicity and embryology, with observations on the population genetics, of the aquacultural echinoid Heliocidaris tuberculata
O'Connor, C., & Mulley, J. C. (1977) · Aquaculture · doi:10.1016/0044-8486(77)90176-4 · Cited by 33 · see citing works
Measure of stress response induced by temperature and salinity changes on hatched larvae of three marine gastropod species
Deschaseaux, E. S. M., Taylor, A. M., & Maher, W. A. (2010) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2010.11.023 · Cited by 33 · see citing works
Climate alert: Climate change monitoring and strategy
You, Y., & Henderson-Sellers, A. (2010) · Cited by 32 · see citing works
Tolerance of juvenile barnacles (Amphibalanus improvisus) to warming and elevated pCO2
Pansch, C., Nasrolahi, A. H., Appelhans, Y. S., & Wahl, M. (2012) · Marine Biology · doi:10.1007/s00227-012-2069-4 · Cited by 31 · see citing works
Legacies in life histories
Padilla, D. K. (2006) · Integrative and Comparative Biology · doi:10.1093/icb/icj029 · Cited by 28 · see citing works
Notes on the egg capsule and variable embryonic development of Nerita melanotragus (Gastropoda: Neritidae)
Przeslawski, R. (2011) · Molluscan Research · doi:10.11646/mr.31.3.2 · Cited by 18 · see citing works
Self-citation
Effects of Varying Temperature and Salinities on Settlement, Growth, and Reproduction of the Wood-Boring Pelecypod, Lyrodus pedicellatus
Eckelbarger, K. J., & Reish, D. J. (1972) · Occidental College Scholar (Occidental College) · Cited by 12 · see citing works

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Multiple Stressors in a Changing World: The Need for an Improved Perspective on Physiological Responses to the Dynamic Marine Environment
Gunderson, A. R., Armstrong, E. J., & Stillman, J. H. (2015) · Annual Review of Marine Science · doi:10.1146/annurev-marine-122414-033953 · Cited by 668 · see citing works
Harmful algal blooms: A climate change co-stressor in marine and freshwater ecosystems
Griffith, A. W., & Gobler, C. J. (2020) · Harmful Algae · doi:10.1016/j.hal.2019.03.008 · Cited by 598 · 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
A review and meta‐analysis of the effects of multiple abiotic stressors on marine embryos and larvae
Przeslawski, R., Byrne, M., & Mellin, C. (2014) · Global Change Biology · doi:10.1111/gcb.12833 · Cited by 514 · see citing works
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Hypoxia and acidification in ocean ecosystems: coupled dynamics and effects on marine life
Gobler, C. J., & Baumann, H. (2016) · Biology Letters · doi:10.1098/rsbl.2015.0976 · Cited by 354 · see citing works
Physiological Responses to Shifts in Multiple Environmental Stressors: Relevance in a Changing World
Todgham, A. E., & Stillman, J. H. (2013) · Integrative and Comparative Biology · doi:10.1093/icb/ict086 · Cited by 352 · see citing works
A roadmap for Antarctic and Southern Ocean science for the next two decades and beyond
Kennicutt, M. C., Chown, S. L., Cassano, J. J., Liggett, D., Peck, L. S., Massom, R. A., Rintoul, S. R., Storey, J. W. V., Vaughan, D. G., Wilson, T. J., et al. (2014) · Antarctic Science · doi:10.1017/s0954102014000674 · Cited by 216 · see citing works
A critical review of the potential impacts of marine seismic surveys on fish & invertebrates
Carroll, A. G., Przeslawski, R., Duncan, A. J., Gunning, M.-E., & Bruce, B. (2016) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2016.11.038 · Cited by 172 · see citing works
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Transgenerational responses of molluscs and echinoderms to changing ocean conditions
Ross, P. M., Parker, L. M., & Byrne, M. (2016) · ICES Journal of Marine Science · doi:10.1093/icesjms/fsv254 · Cited by 163 · see citing works
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Human threats to sandy beaches: A meta-analysis of ghost crabs illustrates global anthropogenic impacts.
Schlacher, T. A., Lucrezi, S., Connolly, R. M., Peterson, C. H., Gilby, B. L., Maslo, B., Olds, A. D., Walker, S. J., Leon, J. X., Huijbers, C. M., et al. (2015) · Estuarine Coastal and Shelf Science · doi:10.1016/j.ecss.2015.11.025 · Cited by 155 · see citing works
The stunting effect of a high CO 2 ocean on calcification and development in sea urchin larvae, a synthesis from the tropics to the poles
Byrne, M., Lamare, M. D., Winter, D. J., Dworjanyn, S. A., & Uthicke, S. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0439 · Cited by 150 · see citing works
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Biological and ecological traits of marine species
Costello, M. J., Claus, S., Dekeyzer, S., Vandepitte, L., Tuama, É. Ó., Lear, D., & Tyler‐Walters, H. (2015) · PeerJ · doi:10.7717/peerj.1201 · Cited by 147 · see citing works
Thermal Plasticity in Insects’ Response to Climate Change and to Multifactorial Environments
Rodrigues, Y. K., & Beldade, P. (2020) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2020.00271 · Cited by 129 · see citing works
Interactive Effects of Ocean Acidification, Elevated Temperature, and Reduced Salinity on Early-Life Stages of the Pacific Oyster
Ko, G. W. K., Dineshram, R., Campanati, C., Chan, V. B. S., Havenhand, J. N., & Thiyagarajan, V. (2014) · Environmental Science & Technology · doi:10.1021/es501611u · Cited by 126 · see citing works
Indirect effects of climate changes on cadmium bioavailability and biological effects in the Mediterranean mussel Mytilus galloprovincialis
Nardi, A., Mincarelli, L. F., Benedetti, M., Fattorini, D., d’Errico, G., & Regoli, F. (2016) · Chemosphere · doi:10.1016/j.chemosphere.2016.11.093 · Cited by 124 · see citing works
Ocean acidification increases the vulnerability of native oysters to predation by invasive snails
Sanford, E., Gaylord, B., Hettinger, A., Lenz, E. A., Meyer, K. S., & Hill, T. M. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.2681 · Cited by 123 · see citing works
Linking the biological impacts of ocean acidification on oysters to changes in ecosystem services: A review
Lemasson, A. J., Fletcher, S., Hall-Spencer, J. M., & Knights, A. M. (2017) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2017.01.019 · Cited by 120 · see citing works
Ocean acidification promotes broad transcriptomic responses in marine metazoans: a literature survey
Strader, M. E., Wong, J. M., & Hofmann, G. E. (2020) · Frontiers in Zoology · doi:10.1186/s12983-020-0350-9 · Cited by 107 · see citing works
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
Wahl, M., Saderne, V., & Sawall, Y. (2015) · Marine and Freshwater Research · doi:10.1071/mf14154 · Cited by 106 · see citing works
Mangrove Ecosystems under Climate Change
Jennerjahn, T. C., Gilman, E. L., Krauss, K. W., de Lacerda, L. D., Nordhaus, I., & Wolanski, E. J. (2017) · Springer eBooks · doi:10.1007/978-3-319-62206-4_7 · Cited by 111 · see citing works
Ocean acidification increases copper toxicity differentially in two key marine invertebrates with distinct acid-base responses
Lewis, C. N., Ellis, R. P., Vernon, E. L., Elliot, K., Newbatt, S., & Wilson, R. W. (2016) · Scientific Reports · doi:10.1038/srep21554 · Cited by 103 · see citing works
Climate change stressors destabilize the microbiome of the Caribbean barrel sponge, Xestospongia muta
Lesser, M. P., Fiore, C. F. C., Slattery, M., & Zaneveld, J. (2015) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2015.11.004 · Cited by 100 · see citing works
Combined Effects of Ocean Warming and Acidification on Copepod Abundance, Body Size and Fatty Acid Content
Garzke, J., Hansen, T., Ismar, S. M. H., & Sommer, U. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0155952 · Cited by 97 · see citing works
Transgenerational exposure of North Atlantic bivalves to ocean acidification renders offspring more vulnerable to low pH and additional stressors
Griffith, A. W., & Gobler, C. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-11442-3 · Cited by 95 · see citing works
Climate-driven changes to ocean circulation and their inferred impacts on marine dispersal patterns
Wilson, L. J., Fulton, C., Hogg, A., Joyce, K., Radford, B., & Fraser, C. (2016) · Global Ecology and Biogeography · doi:10.1111/geb.12456 · Cited by 91 · see citing works
Ocean acidification exerts negative effects during warming conditions in a developing Antarctic fish
Flynn, E. E., Bjelde, B. E., Miller, N. A., & Todgham, A. E. (2015) · Conservation Physiology · doi:10.1093/conphys/cov033 · Cited by 93 · see citing works
Experimental assessments of marine species sensitivities to ocean acidification and co-stressors: how far have we come?
Baumann, H. (2019) · Canadian Journal of Zoology · doi:10.1139/cjz-2018-0198 · Cited by 92 · see citing works
Interactive effects of temperature and pCO 2 on sponges: from the cradle to the grave
Bennett, H. M., Altenrath, C., Woods, L., Davy, S. K., Webster, N. S., & Bell, J. J. (2016) · Global Change Biology · doi:10.1111/gcb.13474 · Cited by 91 · see citing works
Interactive effects of near-future temperature increase and ocean acidification on physiology and gonad development in adult Pacific sea urchin, Echinometra sp. A
Uthicke, S., Liddy, M., Nguyen, H. D., & Byrne, M. (2014) · Coral Reefs · doi:10.1007/s00338-014-1165-y · Cited by 89 · see citing works
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Often Overlooked: Understanding and Meeting the Current Challenges of Marine Invertebrate Conservation
Chen, E. Y.-S. (2021) · Frontiers in Marine Science · doi:10.3389/fmars.2021.690704 · Cited by 87 · see citing works
Current understanding and challenges for oceans in a higher-CO2 world
Hurd, C. L., Lenton, A. A., Tilbrook, B., & Boyd, P. W. (2018) · Nature Climate Change · doi:10.1038/s41558-018-0211-0 · Cited by 85 · see citing works
Effects of ocean warming and acidification on survival, growth and skeletal development in the early benthic juvenile sea urchin (Heliocidaris erythrogramma)
Wolfe, K., Dworjanyn, S. A., & Byrne, M. (2013) · Global Change Biology · doi:10.1111/gcb.12249 · Cited by 84 · see citing works
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Ocean warming and elevated carbon dioxide: multiple stressor impacts on juvenile mussels from southern Chile
Navarro, J. M., Duarte, C., Manríquez, P. H., Lardies, M. A., Torres, R., Acuña, K., Vargas, C. A., & Lagos, N. A. (2016) · ICES Journal of Marine Science · doi:10.1093/icesjms/fsv249 · Cited by 83 · see citing works
The effect of hypoxia on fish schooling
Domenici, P., Steffensen, J. F., & Marras, S. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0236 · Cited by 79 · see citing works
Ocean Warming and CO2-Induced Acidification Impact the Lipid Content of a Marine Predatory Gastropod
Valles-Regino, R., Tate, R. D., Kelaher, B. P., Savins, D., Dowell, A., & Benkendorff, K. (2015) · Marine Drugs · doi:10.3390/md13106019 · Cited by 77 · see citing works
Effects of multiple climate change stressors: ocean acidification interacts with warming, hyposalinity, and low food supply on the larvae of the brooding flat oyster Ostrea angasi
Cole, V. J., Parker, L. M., O'Connor, S. J. M., O’Connor, W. A., Scanes, E., Byrne, M., & Ross, P. M. (2016) · Marine Biology · doi:10.1007/s00227-016-2880-4 · Cited by 78 · see citing works
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Effects of temperature and ocean acidification on shell characteristics of Argopecten purpuratus: implications for scallop aquaculture in an upwelling-influenced area
Lagos, N., Benítez, S., Duarte, C., Lardies, M. A., Broitman, B. R., Tapia, C., Tapia, P., Widdicombe, S., & Vargas, C. A. (2016) · Aquaculture Environment Interactions · doi:10.3354/aei00183 · Cited by 79 · see citing works
The Importance of Natural Acidified Systems in the Study of Ocean Acidification: What Have We Learned?
González-Delgado, S., & Hernández, J. C. (2018) · Advances in marine biology · doi:10.1016/bs.amb.2018.08.001 · Cited by 77 · see citing works
Rethinking our approach to multiple stressor studies in marine environments
Griffen, B. D., Belgrad, B. A., Cannizzo, Z. J., Knotts, E. R., & Hancock, E. R. (2016) · Marine Ecology Progress Series · doi:10.3354/meps11595 · Cited by 80 · see citing works
Molluscs on acid: gastropod shell repair and strength in acidifying oceans
Coleman, D. W., Byrne, M., & Davis, A. R. (2014) · Marine Ecology Progress Series · doi:10.3354/meps10887 · Cited by 75 · see citing works
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Ocean acidification does not impact shell growth or repair of the Antarctic brachiopod Liothyrella uva (Broderip, 1833)
Cross, E. L., Peck, L. S., & Harper, E. M. (2014) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2014.10.013 · Cited by 67 · see citing works
Cadmium stress effects indicating marine pollution in different species of sea urchin employed as environmental bioindicators
Chiarelli, R., Martino, C., & Roccheri, M. C. (2019) · Cell Stress and Chaperones · doi:10.1007/s12192-019-01010-1 · Cited by 67 · see citing works
Fate of Calcifying Tropical Symbiont-Bearing Large Benthic Foraminifera: Living Sands in a Changing Ocean
Doo, S. S., Fujita, K., Byrne, M., & Uthicke, S. (2014) · Biological Bulletin · doi:10.1086/bblv226n3p169 · Cited by 67 · see citing works
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Sea urchins in a high CO2 world: Impacts of climate warming and ocean acidification across life history stages
Byrne, M., & Hernández, J. C. (2020) · Developments in aquaculture and fisheries science · doi:10.1016/b978-0-12-819570-3.00016-0 · Cited by 66 · see citing works
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The challenges of detecting and attributing ocean acidification impacts on marine ecosystems
Doo, S. S., Kealoha, A. K., Andersson, A. J., Cohen, A. L., Hicks, T. L., Johnson, Z. I., Long, M. H., McElhany, P., Mollica, N. R., Shamberger, K. E. F., et al. (2020) · ICES Journal of Marine Science · doi:10.1093/icesjms/fsaa094 · Cited by 65 · see citing works
Effects of ocean acidification on copepods
Wang, M., Jeong, C., Lee, Y. H., & Lee, J. (2018) · Aquatic Toxicology · doi:10.1016/j.aquatox.2018.01.004 · Cited by 66 · see citing works
Season affects strength and direction of the interactive impacts of ocean warming and biotic stress in a coastal seaweed ecosystem
Wahl, M., Werner, F. J., Buchholz, B., Raddatz, S., Graiff, A., Matthiessen, B., Karsten, U., Hiebenthal, C., Hamer, J., Ito, M., et al. (2019) · Limnology and Oceanography · doi:10.1002/lno.11350 · Cited by 64 · see citing works
Differential response to abiotic stress controls species distributions at biogeographic transition zones
Sommer, B., Beger, M., Harrison, P. L., Babcock, R. C., & Pandolfi, J. M. (2017) · Ecography · doi:10.1111/ecog.02986 · Cited by 63 · see citing works
Symbiont transmission in marine sponges: reproduction, development, and metamorphosis
Carrier, T. J., Maldonado, M., Schmittmann, L., Pita, L., Bosch, T. C. G., & Hentschel, U. (2022) · BMC Biology · doi:10.1186/s12915-022-01291-6 · Cited by 58 · see citing works
High sensitivity of embryo-larval stage of the Mediterranean mussel, Mytilus galloprovincialis to metal pollution in combination with temperature increase
Boukadida, K., Bannı, M., Gourvès, P.-Y., & Cachot, J. (2016) · Marine Environmental Research · doi:10.1016/j.marenvres.2016.09.007 · Cited by 62 · see citing works
Impacts of ocean acidification on sea urchin growth across the juvenile to mature adult life-stage transition is mitigated by warming
Dworjanyn, S. A., & Byrne, M. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2017.2684 · Cited by 62 · see citing works
Self-citation
Linking rising pCO2 and temperature to the larval development and physiology of the American lobster (Homarus americanus)
Waller, J. D., Wahle, R. A., Mcveigh, H., & Fields, D. M. (2016) · ICES Journal of Marine Science · doi:10.1093/icesjms/fsw154 · Cited by 61 · see citing works
The Skeleton of Postmetamorphic Echinoderms in a Changing World
Dubois, P. (2014) · Biological Bulletin · doi:10.1086/bblv226n3p223 · Cited by 60 · see citing works
Identifying Thermally-Stressed Adult Green-Lipped Mussels(Perna canaliculusGmelin, 1791)via Metabolomic Profiling*
Dunphy, B. J., Watts, E., & Ragg, N. L. C. (2015) · American Malacological Bulletin · doi:10.4003/006.033.0110 · Cited by 59 · see citing works
Can multi-generational exposure to ocean warming and acidification lead to the adaptation of life history and physiology in a marine metazoan?
Gibbin, E., Chakravarti, L., Jarrold, M. D., Christen, F., Turpin, V., N'Siala, G. M., Blier, P., & Calosi, P. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.149989 · Cited by 61 · see citing works
Marine gametes in a changing ocean: Impacts of climate change stressors on fecundity and the egg
Foo, S. A., & Byrne, M. (2017) · Marine Environmental Research · doi:10.1016/j.marenvres.2017.02.004 · Cited by 59 · see citing works
Self-citation
Warming Influences Mg2+ Content, While Warming and Acidification Influence Calcification and Test Strength of a Sea Urchin
Byrne, M., Smith, A. M., West, S., Collard, M., Dubois, P., Graba‐Landry, A., & Dworjanyn, S. A. (2014) · Environmental Science & Technology · doi:10.1021/es5017526 · Cited by 58 · see citing works
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Environmentally-induced parental or developmental conditioning influences coral offspring ecological performance
Putnam, H. M., Ritson‐Williams, R., Cruz, J. A., Davidson, J. M., & Gates, R. D. (2020) · Scientific Reports · doi:10.1038/s41598-020-70605-x · Cited by 58 · see citing works
Physiological responses to ocean acidification and warming synergistically reduce condition of the common cockle Cerastoderma edule
Ong, E. Z., Briffa, M., Moens, T., & Colen, C. V. (2017) · Marine Environmental Research · doi:10.1016/j.marenvres.2017.07.001 · Cited by 56 · see citing works
Indications of future performance of native and non-native adult oysters under acidification and warming
Lemasson, A. J., Hall-Spencer, J. M., Fletcher, S., Provstgaard-Morys, S., & Knights, A. M. (2018) · Marine Environmental Research · doi:10.1016/j.marenvres.2018.10.003 · Cited by 55 · see citing works
Environmental considerations for subseabed geological storage of CO : A review
Carroll, A. G., Przeslawski, R., Radke, L. C., Black, J. R., Picard, K., Moreau, J. W., Haese, R. R., & Nichol, S. (2013) · Continental Shelf Research · doi:10.1016/j.csr.2013.11.012 · Cited by 54 · see citing works
Self-citation
Ocean warming will mitigate the effects of acidification on calcifying sea urchin larvae (Heliocidaris tuberculata) from the Australian global warming hot spot
Byrne, M., Foo, S. A., Soars, N. A., Wolfe, K., Nguyen, H. D., Hardy, N. A., & Dworjanyn, S. A. (2013) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2013.07.016 · Cited by 53 · see citing works
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Temperature and salinity: two climate change stressors affecting early development of the New Zealand sea urchin Evechinus chloroticus
Delorme, N. J., & Sewell, M. A. (2014) · Marine Biology · doi:10.1007/s00227-014-2480-0 · Cited by 53 · see citing works
Effects of Ocean Acidification and Warming on Sperm Activity and Early Life Stages of the Mediterranean Mussel (Mytilus galloprovincialis)
Vihtakari, M., Hendriks, I. E., Holding, J. M., Renaud, P. E., Duarte, C. M., & Havenhand, J. N. (2013) · Water · doi:10.3390/w5041890 · Cited by 53 · see citing works
No ocean acidification effects on shell growth and repair in the New Zealand brachiopod Calloria inconspicua (Sowerby, 1846)
Cross, E. L., Peck, L. S., Lamare, M. D., & Harper, E. M. (2015) · ICES Journal of Marine Science · doi:10.1093/icesjms/fsv031 · Cited by 51 · see citing works
Alteration of host-pathogen interactions in the wake of climate change – Increasing risk for shellfish associated infections?
Hernroth, B. E., & Baden, S. P. (2017) · Environmental Research · doi:10.1016/j.envres.2017.11.032 · Cited by 52 · see citing works
Biodiversity of coral reef cryptobiota shuffles but does not decline under the combined stressors of ocean warming and acidification
Timmers, M., Jury, C. P., Vicente, J., Bahr, K., Webb, M. K., & Toonen, R. (2021) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2103275118 · Cited by 40 · see citing works
Larvae of the coral eating crown‐of‐thorns starfish, Acanthaster planci in a warmer‐high CO 2 ocean
Kamya, P. Z., Dworjanyn, S. A., Hardy, N. A., Mos, B., Uthicke, S., & Byrne, M. (2014) · Global Change Biology · doi:10.1111/gcb.12530 · Cited by 51 · see citing works
Self-citation
Ocean acidification has little effect on developmental thermal windows of echinoderms from Antarctica to the tropics
Karelitz, S. E., Uthicke, S., Foo, S. A., Barker, M., Byrne, M., Pecorino, D., & Lamare, M. D. (2016) · Global Change Biology · doi:10.1111/gcb.13452 · Cited by 50 · see citing works
Self-citation
Synthesis of Thresholds of Ocean Acidification Impacts on Echinoderms
Bednaršek, N., Calosi, P., Feely, R., Ambrose, R., Byrne, M., Chan, K. Y. K., Dupont, S., Padilla-Gamiño, J., Spicer, J., Kessouri, F., et al. (2021) · Frontiers in Marine Science · doi:10.3389/fmars.2021.602601 · Cited by 38 · see citing works
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Habitat compression and expansion of sea urchins in response to changing climate conditions on the California continental shelf and slope (1994–2013)
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Authors: Byrne, M., & Przeslawski, R.
Affiliations: The University of Sydney (AU)
Corresponding author: Byrne, M.
ORCID: Byrne, M.
Przeslawski, R.
Venue: Integrative and Comparative Biology
Publisher: Oxford University Press (OUP)
Published: 2013-05-22
Volume: 53
Issue: 4
Pages: 582-596
ISSN: 1540-7063 (ISSN-L)
1557-7023
DOI: 10.1093/icb/ict049
OpenAlex: W1987748704
Cited by: 388
References: 97
Citations by year: 2026: 15 · 2025: 21 · 2024: 29 · 2023: 24 · 2022: 30 · 2021: 31 · 2020: 39 · 2019: 32 · 2018: 26 · 2017: 42 · 2016: 40 · 2015: 22 · 2014: 30 · 2013: 7
FWCI: 23.38
Type: journal article
Language: en
Open access: closed
Locations: Integrative and Comparative Biology (publishedVersion)
PubMed (publishedVersion)
Funders: National Science Foundation
Topics: Physical Sciences › Earth and Planetary Sciences › Oceanography › Ocean Acidification Effects and Responses
Physical Sciences › Environmental Science › Ecology › Coral and Marine Ecosystems Studies
Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
Keywords: ocean warming, ocean acidification, hypercapnia, marine benthic invertebrates, life history, larval development, fertilisation (biology), synergistic effect, additive and antagonistic effects, carbonate saturation state, climate change, acclimatization
MeSH terms: Adaptation, Biological, Animals, Calcium Carbonate, Carbon Dioxide, Female, Fertilization, Hydrogen-Ion Concentration, Invertebrates, Life Cycle Stages, Male, Models, Biological, Oceans and Seas, Seawater, Species Specificity, Stress, Physiological, Temperature, Global Warming

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Multistressor impacts of warming and acidification of the ocean on marine invertebrates’ life histories

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