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

The DOI matches its Crossref record; 97 of the 97 references it cites were found in a registry or an index.

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

Open this paper in CoChat — free account

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.

Integrity signals

Registry

Crossref · 10.1093/icb/ict049

Cites

97 of 97 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Ocean Acidification: The Other CO 2 Problem
Doney, S. C., Fabry, V. J., Feely, R. A., & Kleypas, J. A. (2009) · Annual Review of Marine Science · doi:10.1146/annurev.marine.010908.163834 · Cited by 4,173
Climate change impacts on marine ecosystems
Doney, S. C., Ruckelshaus, M., Emmett Duffy, J., Barry, J. P., Chan, F., English, C. A., Galindo, H. M., Grebmeier, J. M., Hollowed, A. B., Knowlton, N., et al. (2012) · Annual Review of Marine Science · doi:10.1146/annurev-marine-041911-111611 · Cited by 3,014
The impacts of climate change in coastal marine systems
Harley, C. D. G., Randall Hughes, A., Hultgren, K. M., Miner, B. G., Sorte, C. J. B., Thornber, C. S., Rodriguez, L. F., Tomanek, L., & Williams, S. L. (2006) · Ecology Letters · doi:10.1111/j.1461-0248.2005.00871.x · Cited by 2,700
Impact of Anthropogenic CO 2 on the CaCO 3 System in the Oceans
Feely, R. A., Sabine, C. L., Lee, K., Berelson, W., Kleypas, J., Fabry, V. J., & Millero, F. J. (2004) · Science · doi:10.1126/science.1097329 · Cited by 2,262
The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’
Somero, G. N. (2010) · Journal of Experimental Biology · doi:10.1242/jeb.037473 · Cited by 1,951
Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems
Pörtner, H.-O. (2010) · Journal of Experimental Biology · doi:10.1242/jeb.037523 · Cited by 1,458
Reproduction of Marine Invertebrates
(1979) · Elsevier eBooks · doi:10.1016/b978-0-12-282505-7.x5001-5 · Cited by 1,268
Shrinking body size as an ecological response to climate change
Sheridan, J. A., & Bickford, D. (2011) · Nature Climate Change · doi:10.1038/nclimate1259 · Cited by 1,117
Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean
Caldeira, K., & Wickett, M. E. (2005) · Journal of Geophysical Research: Oceans · doi:10.1029/2004jc002671 · Cited by 1,040
High-Frequency Dynamics of Ocean pH: A Multi-Ecosystem Comparison
Hofmann, G. E., Smith, J. E., Johnson, K. S., Send, U., Levin, L. A., Micheli, F., Paytan, A., Price, N. N., Peterson, B., Takeshita, Y., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028983 · Cited by 1,014
Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation
O'Connor, M. I., Bruno, J. F., Gaines, S. D., Halpern, B. S., Lester, S. E., Kinlan, B. P., & Weiss, J. M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603422104 · Cited by 924
Synergism and antagonism among multiple stressors
Folt, C. L., Chen, C. Y., Moore, M. V., & Burnaford, J. L. (1999) · Limnology and Oceanography · doi:10.4319/lo.1999.44.3_part_2.0864 · Cited by 879
Juvenile mortality in benthic marine invertebrates
Gosselin, L., & Qian, P. (1997) · Marine Ecology Progress Series · doi:10.3354/meps146265 · Cited by 790
Climate Change and Latitudinal Patterns of Intertidal Thermal Stress
Helmuth, B. S. T., Harley, C. D. G., Halpin, P. M., O’Donnell, M. J., Hofmann, G. E., & Blanchette, C. A. (2002) · Science · doi:10.1126/science.1076814 · Cited by 740
Living on the Edge of Two Changing Worlds: Forecasting the Responses of Rocky Intertidal Ecosystems to Climate Change
Helmuth, B., Mieszkowska, N., Moore, P., & Hawkins, S. J. (2006) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.37.091305.110149 · Cited by 733
Physiological basis for high CO 2 tolerance in marine ectothermic animals: pre-adaptation through lifestyle and ontogeny?
Melzner, F., Gutowska, M. A., Langenbuch, M., Dupont, S., Lucassen, M., Thorndyke, M. C., Bleich, M., & Pörtner, H. (2009) · Biogeosciences · doi:10.5194/bg-6-2313-2009 · Cited by 682
Larval experience and latent effects--metamorphosis is not a new beginning
Pechenik, J. A. (2006) · Integrative and Comparative Biology · doi:10.1093/icb/icj028 · Cited by 599
Warming-induced reductions in body size are greater in aquatic than terrestrial species
Forster, J., Hirst, A. G., & Atkinson, D. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1210460109 · Cited by 557
The Effect of Ocean Acidification on Calcifying Organisms in Marine Ecosystems: An Organism-to-Ecosystem Perspective
Hofmann, G. E., Barry, J., Edmunds, P. J., Gates, R. D., Hutchins, D. A., Klinger, T., & Sewell, M. A. (2010) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev.ecolsys.110308.120227 · Cited by 555
Coral-associated invertebrates
Stella, J. S., Pratchett, M. S., Hutchings, P., & Jones, G. P. (2011) · Oceanography and Marine Biology/Oceanography and marine biology - an annual review · doi:10.1201/b11009-3 · Cited by 522
Food availability outweighs ocean acidification effects in juvenile Mytilus edulis : laboratory and field experiments
Thomsen, J., Casties, I., Pansch, C., Körtzinger, A., & Melzner, F. (2013) · Global Change Biology · doi:10.1111/gcb.12109 · Cited by 446
Adult exposure influences offspring response to ocean acidification in oysters
Parker, L. M., Ross, P. M., O’Connor, W. A., Borysko, L., Raftos, D. A., & Pörtner, H. (2011) · Global Change Biology · doi:10.1111/j.1365-2486.2011.02520.x · Cited by 441
Elevated level of carbon dioxide affects metabolism and shell formation in oysters Crassostrea virginica (Gmelin)
Beniash, E., Ivanina, A. V., Lieb, N., Kurochkin, I. O., & Sokolova, I. M. (2010) · Marine Ecology Progress Series · doi:10.3354/meps08841 · Cited by 405
Embryo stability and vulnerability in an always changing world
Hamdoun, A. M., & Epel, D. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610108104 · Cited by 401
Impact of near-future ocean acidification on echinoderms
Dupont, S., Ortega‐Martinez, O., & Thorndyke, M. C. (2010) · Ecotoxicology · doi:10.1007/s10646-010-0463-6 · Cited by 399
Predicting the Response of Molluscs to the Impact of Ocean Acidification
Parker, L. M., Ross, P. M., O’Connor, W. A., Pörtner, H., Scanes, E., & Wright, J. M. (2013) · Biology · doi:10.3390/biology2020651 · Cited by 371
Recent Antarctic Peninsula warming relative to Holocene climate and ice-shelf history
Mulvaney, R., Abram, N. J., Hindmarsh, R. C. A., Arrowsmith, C., Fleet, L., Triest, J., Sime, L. C., Alemany, O., & Foord, S. (2012) · Nature · doi:10.1038/nature11391 · Cited by 356
Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis
Dupont, S., Dorey, N., Stumpp, M., Melzner, F., & Thorndyke, M. C. (2012) · Marine Biology · doi:10.1007/s00227-012-1921-x · Cited by 347
Beyond corals and fish: the effects of climate change on noncoral benthic invertebrates of tropical reefs
Przeslawski, R., Ahyong, S. T., Byrne, M., Wörheide, G., & Hutchings, P. (2008) · Global Change Biology · doi:10.1111/j.1365-2486.2008.01693.x · Cited by 337
Self-citation
All males are not created equal: Fertility differences depend on gamete recognition polymorphisms in sea urchins
Palumbi, S. R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.22.12632 · Cited by 323
Extensive dissolution of live pteropods in the Southern Ocean
Bednaršek, N., Tarling, G. A., Bakker, D. C. E., Fielding, S., Jones, E. M., Venables, H. J., Ward, P., Kuzirian, A. M., Lézé, B., Feely, R. A., et al. (2012) · Nature Geoscience · doi:10.1038/ngeo1635 · Cited by 321
Effect of increased atmospheric CO2 on shallow water marine benthos
Shirayama, Y., & Thornton, H. (2005) · Journal of Geophysical Research Atmospheres · doi:10.1029/2004jc002618 · Cited by 311
Impact of Ocean Warming and Ocean Acidification on Larval Development and Calcification in the Sea Urchin Tripneustes gratilla
Brennand, H. S., Soars, N. A., Dworjanyn, S. A., Davis, A. R., & Byrne, M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0011372 · Cited by 307
Self-citation
Observed climate change in Australian marine and freshwater environments
Lough, J., & Hobday, A. J. (2011) · Marine and Freshwater Research · doi:10.1071/mf10272 · Cited by 303
Temperature, but not pH, compromises sea urchin fertilization and early development under near-future climate change scenarios
Byrne, M., Ho, M. A., Selvakumaraswamy, P., Nguyen, H. D., Dworjanyn, S. A., & Davis, A. R. (2009) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2008.1935 · Cited by 298
Self-citation
Projected climate change in Australian marine and freshwater environments
Hobday, A. J., & Lough, J. (2011) · Marine and Freshwater Research · doi:10.1071/mf10302 · Cited by 292
Acidified seawater impacts sea urchin larvae pH regulatory systems relevant for calcification
Stumpp, M., Hu, M. Y., Melzner, F., Gutowska, M. A., Dorey, N., Himmerkus, N., Holtmann, W. C., Dupont, S., Thorndyke, M. C., & Bleich, M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1209174109 · Cited by 283
Effects of Elevated Temperature and Carbon Dioxide on the Growth and Survival of Larvae and Juveniles of Three Species of Northwest Atlantic Bivalves
Talmage, S. C., & Gobler, C. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0026941 · Cited by 279
Global change ecotoxicology: Identification of early life history bottlenecks in marine invertebrates, variable species responses and variable experimental approaches
Byrne, M. (2011) · Marine Environmental Research · doi:10.1016/j.marenvres.2011.10.004 · Cited by 278
Self-citation
Transcriptomic response of sea urchin larvaeStrongylocentrotus purpuratusto CO2-driven seawater acidification
Todgham, A. E., & Hofmann, G. E. (2009) · Journal of Experimental Biology · doi:10.1242/jeb.032540 · Cited by 269
Comparing the effect of elevated pCO2 and temperature on the fertilization and early development of two species of oysters
Parker, L. M., Ross, P. M., & O’Connor, W. A. (2010) · Marine Biology · doi:10.1007/s00227-010-1508-3 · Cited by 236
Persistent carry‐over effects of planktonic exposure to ocean acidification in the Olympia oyster
Hettinger, A., Sanford, E., Hill, T. M., Russell, A. D., Sato, K. N., Hoey, J. A., Forsch, M., Page, H. N., & Gaylord, B. (2012) · Ecology · doi:10.1890/12-0567.1 · Cited by 220
Ocean acidification impacts multiple early life history processes of the Caribbean coral Porites astreoides
Albright, R., & Langdon, C. (2011) · Global Change Biology · doi:10.1111/j.1365-2486.2011.02404.x · Cited by 217
Functional Consequences of Phenotypic Plasticity in Echinoid Larvae
Hart, M. W., & Strathmann, R. R. (1994) · Biological Bulletin · doi:10.2307/1542275 · Cited by 204
Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean
Byrne, M., Ho, M. A., Wong, E., Soars, N. A., Selvakumaraswamy, P., Brennand, H. S., Dworjanyn, S. A., & Davis, A. R. (2010) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2010.2404 · Cited by 204
Self-citation
The Impact of Ocean Acidification on Reproduction, Early Development and Settlement of Marine Organisms
Ross, P. M., Parker, L. M., O’Connor, W. A., & Bailey, E. A. (2011) · Water · doi:10.3390/w3041005 · Cited by 199
Review of climate change impacts on marine aquaculture in the UK and Ireland
Callaway, R., Shinn, A. P., Grenfell, S. E., Bron, J. E., Burnell, G., Cook, E., Crumlish, M., Culloty, S. C., Davidson, K., Ellis, R. P., et al. (2012) · Aquatic Conservation Marine and Freshwater Ecosystems · doi:10.1002/aqc.2247 · Cited by 198
Coral growth with thermal stress and ocean acidification: lessons from the eastern tropical Pacific
Manzello, D. P. (2010) · Coral Reefs · doi:10.1007/s00338-010-0623-4 · Cited by 187
The Importance of Physiological Limits in Determining Biogeographical Range Shifts due to Global Climate Change: The Heat‐Shock Response
Tomanek, L. (2008) · Physiological and Biochemical Zoology · doi:10.1086/590163 · Cited by 172
The influence of multiple environmental stressors on susceptibility to parasites: An experimental determination with oysters
Lenihan, H. S., Micheli, F., Shelton, S. W., & Peterson, C. H. (1999) · Limnology and Oceanography · doi:10.4319/lo.1999.44.3_part_2.0910 · Cited by 167
Coral Larvae under Ocean Acidification: Survival, Metabolism, and Metamorphosis
Nakamura, M., Ohki, S., Suzuki, A., & Sakai, K. (2011) · PLoS ONE · doi:10.1371/journal.pone.0014521 · Cited by 166
Elevated Temperature Affects Development, Survivorship, and Settlement of the Elkhorn Coral, Acropora palmata (Lamarck 1816)
Randall, C. J., & Szmant, A. M. (2009) · Biological Bulletin · doi:10.1086/bblv217n3p269 · Cited by 154
Effects of ocean acidification and warming on the larval development of the spider crab Hyas araneus from different latitudes (54° vs. 79°N)
Walther, K., Anger, K., & Pörtner, H. (2010) · Marine Ecology Progress Series · doi:10.3354/meps08807 · Cited by 151
Effects of ocean acidification over the life history of the barnacle Amphibalanus amphitrite
McDonald, M., McClintock, J. B., Amsler, C. D., Rittschof, D., Angus, R. A., Orihuela, B., & Lutostanski, K. (2009) · Marine Ecology Progress Series · doi:10.3354/meps08099 · Cited by 151
Synergistic effects associated with climate change and the development of rocky shore molluscs
Przeslawski, R., Davis, A. R., & Benkendorff, K. (2005) · Global Change Biology · doi:10.1111/j.1365-2486.2005.00918.x · Cited by 148
Self-citation
In situ estimates of larval development and mortality in the New Zealand sea urchin Evechinus chloroticus (Echinodermata:Echinoidea)
Lamare, M. D., & Barker, M. (1999) · Marine Ecology Progress Series · doi:10.3354/meps180197 · Cited by 148
A corrosive concoction: The combined effects of ocean warming and acidification on the early growth of a stony coral are multiplicative
Anlauf, H., D’Croz, L., & O’Dea, A. (2010) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2010.11.009 · Cited by 135
Adaptive Capacity of the Habitat Modifying Sea Urchin Centrostephanus rodgersii to Ocean Warming and Ocean Acidification: Performance of Early Embryos
Foo, S. A., Dworjanyn, S. A., Poore, A. G. B., & Byrne, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042497 · Cited by 135
Self-citation
Fertilization in a suite of coastal marine invertebrates from SE Australia is robust to near-future ocean warming and acidification
Byrne, M., Soars, N. A., Ho, M. A., Wong, E., McElroy, D. J., Selvakumaraswamy, P., Dworjanyn, S. A., & Davis, A. R. (2010) · Marine Biology · doi:10.1007/s00227-010-1474-9 · Cited by 134
Self-citation
Sea urchin fertilization in a warm, acidified and high pCO2 ocean across a range of sperm densities
Byrne, M., Soars, N. A., Selvakumaraswamy, P., Dworjanyn, S. A., & Davis, A. R. (2009) · Marine Environmental Research · doi:10.1016/j.marenvres.2009.10.014 · Cited by 127
Self-citation
Relative influences of ocean acidification and temperature on intertidal barnacle post-larvae at the northern edge of their geographic distribution
Findlay, H. S., Kendall, M. A., Spicer, J. I., & Widdicombe, S. (2009) · Estuarine Coastal and Shelf Science · doi:10.1016/j.ecss.2009.11.036 · Cited by 119
Reviewing the Effects of Ocean Acidification on Sexual Reproduction and Early Life History Stages of Reef-Building Corals
Albright, R. (2011) · Journal of Marine Biology · doi:10.1155/2011/473615 · Cited by 117
Post-larval development of two intertidal barnacles at elevated CO2 and temperature
Findlay, H. S., Kendall, M. A., Spicer, J. I., & Widdicombe, S. (2009) · Marine Biology · doi:10.1007/s00227-009-1356-1 · Cited by 115
Marine bivalve shell geochemistry and ultrastructure from modern low pH environments: environmental effect versus experimental bias
Hahn, S., Rodolfo‐Metalpa, R., Griesshaber, E., Schmahl, W. W., Buhl, D., Hall-Spencer, J. M., Baggini, C., Fehr, K. T., & Immenhauser, A. (2012) · Biogeosciences · doi:10.5194/bg-9-1897-2012 · Cited by 115
Size-Specific Predation on Marine Invertebrate Larvae
Allen, J. D. (2008) · Biological Bulletin · doi:10.2307/25066658 · Cited by 112
Projected Near-Future Levels of Temperature and pCO2 Reduce Coral Fertilization Success
Albright, R., & Mason, B. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056468 · Cited by 106
Individual Variability in Reproductive Success Determines Winners and Losers under Ocean Acidification: A Case Study with Sea Urchins
Schlegel, P. N., Havenhand, J. N., Gillings, M. R., & Williamson, J. E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0053118 · Cited by 106
Elevated temperature elicits greater effects than decreased pH on the development, feeding and metabolism of northern shrimp (Pandalus borealis) larvae
Arnberg, M., Calosi, P., Spicer, J. I., Tandberg, A. H. S., Nilsen, M., Westerlund, S. F. G., & Bechmann, R. K. (2012) · Marine Biology · doi:10.1007/s00227-012-2072-9 · Cited by 104
Relationships between spawning date and larval development time for benthic marine invertebrates: a modeling approach
Reitzel, A. M., Miner, B. G., & McEdward, L. R. (2004) · Marine Ecology Progress Series · doi:10.3354/meps280013 · Cited by 95
Combined effects of two ocean change stressors, warming and acidification, on fertilization and early development of the Antarctic echinoid Sterechinus neumayeri
Ericson, J. A., Ho, M., Miskelly, A. D., King, C. K., Virtue, P., Tilbrook, B., & Byrne, M. (2011) · Polar Biology · doi:10.1007/s00300-011-1150-7 · Cited by 95
Self-citation
Acid–base balance and metabolic response of the sea urchin Paracentrotus lividus to different seawater pH and temperatures
Catarino, A. I., Bauwens, M., & Dubois, P. (2012) · Environmental Science and Pollution Research · doi:10.1007/s11356-012-0743-1 · Cited by 91
Overview of phenotypic plasticity in echinoid larvae, ‘Echinopluteus transversus’ type vs. typical echinoplutei
Soars, N. A., Prowse, T. A. A., & Byrne, M. (2009) · Marine Ecology Progress Series · doi:10.3354/meps07848 · Cited by 89
Self-citation
Vulnerability of the calcifying larval stage of the Antarctic sea urchin Sterechinus neumayeri to near‐future ocean acidification and warming
Byrne, M., Ho, M. A., Koleits, L., Sedran-Price, C., King, C. K., Virtue, P., Tilbrook, B., & Lamare, M. D. (2013) · Global Change Biology · doi:10.1111/gcb.12190 · Cited by 88
Self-citation
Temperature affects the early life history stages of corals more than near future ocean acidification
Chua, C. M., Leggat, W. P., Moya, A., & Baird, A. (2012) · Marine Ecology Progress Series · doi:10.3354/meps10077 · Cited by 84
Seawater acidification by CO2 in a coastal lagoon environment: Effects on life history traits of juvenile mussels Mytilus galloprovincialis
Range, P., Piló, D., Ben‐Hamadou, R., Chı́charo, L. M. Z., Matias, D. D. C. C., Joaquim, S., Oliveira, A. P., & Chı́charo, L. M. Z. (2012) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2012.05.010 · Cited by 79
Noncalcifying larvae in a changing ocean: warming, not acidification/hypercapnia, is the dominant stressor on development of the sea star M eridiastra calcar
Nguyen, H. D., Doo, S. S., Soars, N. A., & Byrne, M. (2012) · Global Change Biology · doi:10.1111/j.1365-2486.2012.02714.x · Cited by 67
Self-citation
Respiratory response of the intertidal seastar Parvulastra exigua to contemporary and near-future pulses of warming and hypercapnia
McElroy, D. J., Nguyen, H. D., & Byrne, M. (2012) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2012.02.003 · Cited by 62
Self-citation
Differences in Temperature Dependence of Early Development of Sea Urchins with Different Growing Seasons
FUJISAWA, H. (1989) · Biological Bulletin · doi:10.2307/1541576 · Cited by 59
SIMULTANEOUS POSITIVE AND NEGATIVE FREQUENCY-DEPENDENT SELECTION ON SPERM BINDIN, A GAMETE RECOGNITION PROTEIN IN THE SEA URCHINSTRONGYLOCENTROTUS PURPURATUS
Levitan, D. R., & Stapper, A. P. (2009) · Evolution · doi:10.1111/j.1558-5646.2009.00850.x · Cited by 57
Juvenile growth of the tropical sea urchin Lytechinus variegatus exposed to near-future ocean acidification scenarios
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 56
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
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
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
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
Self-citation
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 48
Self-citation
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
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
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
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
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
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
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
Climate alert: Climate change monitoring and strategy
You, Y., & Henderson-Sellers, A. (2010) · Cited by 32
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
Legacies in life histories
Padilla, D. K. (2006) · Integrative and Comparative Biology · doi:10.1093/icb/icj029 · Cited by 28
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
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

Flagged first, then by citations

Research works printed but not linked: 13

2011, J MAR BIOL, 2011, 473615
2012, Journal of Experimental Marine Biology and Ecology, 426, 12
2012, GLOB CHANGE BIOL, 19, 373
2011, OCEANOGR MAR BIOL ANN REV, 49, 1
2000, J SHELLFISH RES, 19, 883
2010, Ecotoxicology (London, England), 19, 440
1972, BULL SOUTH CALIF ACAD SCI, 71, 116
2011, Polar Biology, 35, 1027
1997, Marine Ecology. Progress Series (Halstenbek), 146, 264
2012, Journal of Experimental Marine Biology and Ecology, 416417, 1
2012, MOLLUSCAN RES, 31, 152
2012, Journal of Experimental Marine Biology and Ecology, 424, 89
2012, MOLLUSCAN RES, 32, 177

Sorted by citations

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 718
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
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
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 547
Self-citation
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 all 388

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

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

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

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks