Direct and latent effects of ocean acidification on the transition of a sea urchin from planktonic larva to benthic juvenile
Kwiatkowski, L. et al. Twenty-first century ocean warming, acidification, deoxygenation, and upper-ocean nutrient and primary production decline from CMIP6 model projections. Biogeosciences 17, 3439–3470 (2020).ADS
CAS
Google Scholar
Intergovernmental Panel on Climate Change. Climate Change 2013: 5th Assessment Report of the Intergovernmental Panel on Climate Change (Cambridge University Press, 2013).
Google Scholar
Torres, O., Kwiatkowski, L., Sutton, A. J., Dorey, N. & Orr, J. C. Characterizing mean and extreme diurnal variability of ocean CO2 system variables across marine environments. Geophys. Res. Lett. 48, 2 (2021).
Google Scholar
Dorey, N., Lançon, P., Thorndyke, M. & Dupont, S. Assessing physiological tipping point of sea urchin larvae exposed to a broad range of pH. Glob. Change Biol. 19, 3355–3367 (2013).
Google Scholar
Hauri, C. et al. Spatiotemporal variability and long-term trends of ocean acidification in the California current system. Biogeosci. Discuss. 9, 10371–10428 (2012).ADS
Google Scholar
Dupont, S. & Pörtner, H.-O. A snapshot into ocean acidification research. Mar. Biol. 160, 1765–1771 (2013).CAS
Google Scholar
Dupont, S. & Thorndyke, M. Chapter: Direct impacts of near-future ocean acidification on sea urchins. in Climate Change Perspective from the Atlantic: Past, Present and Future (eds. Fernández-Palacios, J. et al.) 461–485 (2013).Byrne, M. & Hernández, J. C. Chapter 16: Sea urchins in a high CO2 world: Impacts of climate warming and ocean acidification across life history stages. in Developments in Aquaculture and Fisheries Science vol. 43 281–297 (Elsevier, 2020).Kroeker, K. J., Kordas, R. L., Crim, R. N. & Singh, G. G. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett. 13, 1419–1434 (2010).PubMed
Google Scholar
L. Kelley, A., J. Lunden, J., 1 Ocean Acidification Research Center, College of Fisheries and Ocean Sciences, University of Alaska, Fairbanks, Fairbanks, AK, 99775, USA, & 2 Haverford College, Haverford, PA, 19041, USA. Meta-analysis identifies metabolic sensitivities to ocean acidification. AIMS Environ. Sci. 4, 709–729 (2017).Stumpp, M. et al. Acidified seawater impacts sea urchin larvae pH regulatory systems relevant for calcification. Proc. Natl. Acad. Sci. U. S. A. 109, 18192–18197 (2012).ADS
CAS
PubMed
PubMed Central
Google Scholar
Stumpp, M. et al. Digestion in sea urchin larvae impaired under ocean acidification. Nat. Clim. Change 3, 1044–1049 (2013).ADS
CAS
Google Scholar
Runcie, D. E. et al. Genomic characterization of the evolutionary potential of the sea urchin Strongylocentrotus droebachiensis facing ocean acidification. Genome Biol. Evol. 8, 272 (2017).
Google Scholar
Sewell, M. Utilization of lipids during early development of the sea urchin Evechinus chloroticus. Mar. Ecol. Prog. Ser. 304, 133–142 (2005).ADS
CAS
Google Scholar
Lucas, M. I., Walker, G., Holland, D. L. & Crisp, D. J. An energy budget for the free-swimming and metamorphosing larvae of Balanus balanoides (Crustacea: Cirripedia). Mar. Biol. 55, 221–229 (1979).
Google Scholar
Shilling, F. M., Hoegh-Guldberg, O. & Manahan, D. T. Sources of energy for increased metabolic demand during metamorphosis of the abalone Haliotis rufescens (Mollusca). Biol. Bull. 191, 402–412 (1996).CAS
PubMed
Google Scholar
Meidel, S. K. & Scheibling, R. E. Effects of food type and ration on reproductive maturation and growth of the sea urchin Strongylocentrotus droebachiensis. Mar. Biol. 134, 155–166 (1999).
Google Scholar
Pearce, C. M. & Scheibling, R. E. Induction of metamorphosis of larvae of the green sea urchin, Strongylocentrotus droebachiensis by coralline red algae. Biol. Bull. 179, 304–311 (1990).CAS
PubMed
Google Scholar
Gosselin, P. & Jangoux, M. From competent larva to exotrophic juvenile: a morphofunctional study of the perimetamorphic period of Paracentrotus lividus (Echinodermata, Echinoida). Zoomorphology 118, 31–43 (1998).
Google Scholar
Hinegardner, R. T. Growth and development of the laboratory cultured sea urchin. Biol. Bull. 137, 465–475 (1969).CAS
PubMed
Google Scholar
Strathmann, R. R. Length of pelagic period in echinoderms with feeding larvae from the Northeast Pacific. J. Exp. Biol. Ecol. 34, 23–27 (1978).
Google Scholar
Byrne, M. et al. Unshelled abalone and corrupted urchins: Development of marine calcifiers in a changing ocean. Proc. Biol. Sci. 278, 2376–2383 (2011).PubMed
Google Scholar
Dupont, S., Dorey, N., Stumpp, M., Melzner, F. & Thorndyke, M. Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Mar. Biol. 160, 1835–1843 (2013).CAS
Google Scholar
Uthicke, S. et al. Impacts of ocean acidification on early life-history stages and settlement of the coral-eating sea star Acanthaster planci. PLoS ONE 8, e82938 (2013).ADS
PubMed
PubMed Central
Google Scholar
Dupont, S., Lundve, B. & Thorndyke, M. Near future ocean acidification increases growth rate of the lecithotrophic larvae and juveniles of the sea star Crossaster papposus. J. Exp. Zool. Mol. Dev. Evol. 314, 382–389 (2010).
Google Scholar
Lim, Y.-K., Dang, X. & Thiyagarajan, V. Transgenerational responses to seawater pH in the edible oyster, with implications for the mariculture of the species under future ocean acidification. Sci. Total Environ. 782, 146704 (2021).ADS
CAS
PubMed
Google Scholar
Hettinger, A. et al. Persistent carry-over effects of planktonic exposure to ocean acidification in the Olympia oyster. Ecology 93, 2758–2768 (2012).PubMed
Google Scholar
Hettinger, A. et al. Larval carry-over effects from ocean acidification persist in the natural environment. Glob. Change Biol. https://doi.org/10.1111/gcb.12307 (2013).Article
Google Scholar
Albright, R. & Langdon, C. Ocean acidification impacts multiple early life history processes of the Caribbean coral Porites astreoides. Glob. Change Biol. 17, 2478–2487 (2011).ADS
Google Scholar
Yuan, X. et al. Elevated CO2 delays the early development of scleractinian coral Acropora gemmifera. Sci. Rep. 8, 2787 (2018).ADS
PubMed
PubMed Central
Google Scholar
Maboloc, E. A. & Chan, K. Y. K. Parental whole life cycle exposure modulates progeny responses to ocean acidification in slipper limpets. Glob. Change Biol. 2, 15647. https://doi.org/10.1111/gcb.15647 (2021).Article
Google Scholar
Mos, B., Byrne, M. & Dworjanyn, S. A. Effects of low and high pH on sea urchin settlement, implications for the use of alkali to counter the impacts of acidification. Aquaculture 528, 735618 (2020).CAS
Google Scholar
Harianto, J., Aldridge, J., Torres Gabarda, S. A., Grainger, R. J. & Byrne, M. Impacts of acclimation in warm-low pH conditions on the physiology of the sea urchin Heliocidaris erythrogramma and carryover effects for juvenile offspring. Front. Mar. Sci. 7, 588938 (2021).
Google Scholar
Houlihan, E. P., Espinel-Velasco, N., Cornwall, C. E., Pilditch, C. A. & Lamare, M. D. Diffusive boundary layers and ocean acidification: Implications for sea urchin settlement and growth. Front. Mar. Sci. 7, 577562 (2020).
Google Scholar
Norderhaug, K. M. & Christie, H. C. Sea urchin grazing and kelp re-vegetation in the NE Atlantic. Mar. Biol. Res. 5, 515–528 (2009).
Google Scholar
Dickson, A., Sabine, C. L. & Christian, J. R. Guide to best practices for ocean CO2 measurements. (PICES Special Publication 3;191 pp, 2007).Lavigne, H. & Gattuso, J.-P. seacarb: seawater carbonate chemistry with R. R package version 2.4. http://CRAN.R-project.org/package=seacarb. (2011).R Core Team. R: A language and environment for statistical computing. R: A language and environment for statistical computing (2017).Guillard, R. R. L. & Ryther, J. H. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can. J. Microbiol. 8, 229–239 (1962).CAS
PubMed
Google Scholar
Stumpp, M., Wren, J., Melzner, F., Thorndyke, M. & Dupont, S. CO2 induced seawater acidification impacts sea urchin larval development I: Elevated metabolic rates decrease scope for growth and induce developmental delay. Comp. Biochem. Physiol. Mol. Integr. Physiol. 160, 331–340 (2011).CAS
Google Scholar
His, E., Heyvang, I., Geffard, O. & De Montaudouin, X. A comparison between oyster (Crassostrea gigas) and sea urchin (Paracentrotus lividus) larval bioassays for toxicological studies. Water Res. 33, 1706–1718 (1999).CAS
Google Scholar
U. S. National Institutes of Health, Bethesda, Maryland, U. ImageJ, Rasband, W.S., http://imagej.nih.gov/ij/.Smith, M. M., Cruz Smith, L., Cameron, R. A. & Urry, L. The larval stages of the sea urchin, Strongylocentrotus purpuratus. J. Morphol. 269, 713–733 (2008).PubMed
Google Scholar
Kahm, M., Hasenbrink, G., Lichtenberg-Frate, H., Ludwig, J. & Kschischo, M. grofit: Fitting Biological Growth Curves with R. J. Stat. Softw., 33(7), 1–21. URL http://www.jstatsoft.org/v33/i07/. (2010).Pinheiro, J., Bates, D., & R-core. Package ‘nlme’: Linear and Nonlinear Mixed Effects Models. Cran-R (2018).Pan, T.-C.F., Applebaum, S. L. & Manahan, D. T. Experimental ocean acidification alters the allocation of metabolic energy. Proc. Natl. Acad. Sci. U. S. A. 112, 4696–4701 (2015).ADS
CAS
PubMed
PubMed Central
Google Scholar
Jager, T., Ravagnan, E. & Dupont, S. Near-future ocean acidification impacts maintenance costs in sea-urchin larvae: Identification of stress factors and tipping points using a DEB modelling approach. J. Exp. Mar. Biol. Ecol. 474, 11–17 (2016).
Google Scholar
Hoegh-Guldberg, O. & Emlet, R. B. Energy use during the development of a lecithotrophic and a planktotrophic echinoid. Biol. Bull. 192, 27–40 (1997).CAS
PubMed
Google Scholar
Vaïtilingon, D. et al. Effects of delayed metamorphosis and food rations on the perimetamorphic events in the echinoid Paracentrotus lividus (Lamarck, 1816) (Echinodermata). J. Exp. Mar. Biol. Ecol. 262, 41–60 (2001).
Google Scholar
García, E., Clemente, S. & Hernández, J. C. Ocean warming ameliorates the negative effects of ocean acidification on Paracentrotus lividus larval development and settlement. Mar. Environ. Res. 110, 61–68 (2015).PubMed
Google Scholar
Wangensteen, O. S., Dupont, S., Casties, I., Turon, X. & Palacín, C. Some like it hot: Temperature and pH modulate larval development and settlement of the sea urchin Arbacia lixula. J. Exp. Mar. Biol. Ecol. 449, 304–311 (2013).
Google Scholar
García, E., Clemente, S. & Hernández, J. C. Effects of natural current pH variability on the sea urchin Paracentrotus lividus larvae development and settlement. Mar. Environ. Res. 139, 11–18 (2018).PubMed
Google Scholar
Marshall, D. J. & Keough, M. J. Variation in the dispersal potential of non-feeding invertebrate larvae: The desperate larva hypothesis and larval size. Mar. Ecol. Prog. Ser. 255, 145–153 (2003).ADS
Google Scholar
Huggett, M. J., Williamson, J. E., de Nys, R., Kjelleberg, S. & Steinberg, P. D. Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae. Oecologia 149, 604–619 (2006).ADS
PubMed
Google Scholar
Espinel-Velasco, N., Agüera, A. & Lamare, M. Sea urchin larvae show resilience to ocean acidification at the time of settlement and metamorphosis. Mar. Environ. Res. 159, 104977 (2020).CAS
PubMed
Google Scholar
Lamare, M. & Barker, M. Settlement and recruitment of the New Zealand sea urchin Evechinus chloroticus. Mar. Ecol. Prog. Ser. 218, 153–166 (2001).ADS
Google Scholar
Martin, S. et al. Early development and molecular plasticity in the Mediterranean sea urchin Paracentrotus lividus exposed to CO2-driven acidification. J. Exp. Biol. 214, 1357–1368 (2011).CAS
PubMed
Google Scholar
Vargas, C. A. et al. Species-specific responses to ocean acidification should account for local adaptation and adaptive plasticity. Nat. Ecol. Evol. 1, 0084 (2017).
Google Scholar
Espinel-Velasco, N. et al. Effects of ocean acidification on the settlement and metamorphosis of marine invertebrate and fish larvae: a review. Mar. Ecol. Prog. Ser. 606, 237–257 (2018).ADS
Google Scholar
Briffa, M., de la Haye, K. & Munday, P. L. High CO2 and marine animal behaviour: potential mechanisms and ecological consequences. Mar. Pollut. Bull. 64, 1519–1528 (2012).CAS
PubMed
Google Scholar
Gaylord, B. et al. Ocean acidification through the lens of ecological theory. Ecology 96, 3–15 (2015).PubMed
Google Scholar More