The stunting effect of a high CO2 ocean on calcification and development in sea urchin larvae, a synthesis from the tropics to the poles

Abstract

The stunting effect of ocean acidification on development of calcifying invertebrate larvae has emerged as a significant effect of global change. We assessed the arm growth response of sea urchin echinoplutei, here used as a proxy of larval calcification, to increased seawater acidity/pCO2 and decreased carbonate mineral saturation in a global synthesis of data from 15 species. Phylogenetic relatedness did not influence the observed patterns. Regardless of habitat or latitude, ocean acidification impedes larval growth with a negative relationship between arm length and increased acidity/pCO2 and decreased carbonate mineral saturation. In multiple linear regression models incorporating these highly correlated parameters, pCO2 exerted the greatest influence on decreased arm growth in the global dataset and also in the data subsets for polar and subtidal species. Thus, reduced growth appears largely driven by organism hypercapnia. For tropical species, decreased carbonate mineral saturation was most important. No single parameter played a dominant role in arm size reduction in the temperate species. For intertidal species, the models were equivocal. Levels of acidification causing a significant (approx. 10-20+%) reduction in arm growth varied between species. In 13 species, reduction in length of arms and supporting skeletal rods was evident in larvae reared in near-future (pCO2 800+ µatm) conditions, whereas greater acidification (pCO2 1000+ µatm) reduced growth in all species. Although multi-stressor studies are few, when temperature is added to the stressor mix, near-future warming can reduce the negative effect of acidification on larval growth. Broadly speaking, responses of larvae from across world regions showed similar trends despite disparate phylogeny, environments and ecology. Larval success may be the bottleneck for species success with flow-on effects for sea urchin populations and marine ecosystems.

Keywords: calcifying larvae; echinopluteus; global change; ocean acidification; ocean warming.

Figure 1.

Temperature and pH variation in the shallow subtidal habitat (grey line) of the sea urchin Heliocidaris tuberculata (Lamarck, 1816) and the low intertidal tide pool habitat (black line) of the sea star Meridiastra calcar, Sydney, Australia (June 2011–June 2012), showing the seasonal cycle and the warm/cold temperature spikes experienced by these species. Tide pool temperature as recorded by in situ loggers (Thermodata iBCod G, data collected every 20 min) can change daily by 8–10°C. The gaps are when loggers were lost [25,26]. Seawater chemistry at pre-dawn and pre-sunset low spring tides indicates extreme conditions in the shallow subtidal (yellow (grey) diamonds; pH_t (total scale) range: 7.88–8.25; pCO₂: 219–614 μatm) and low intertidal (red (black) diamonds; pH_t range: 7.86–8.27; pCO₂: 209–659 μatm). pH_t and pCO₂ were determined from analysis of total alkalinity (measured by potentiometric titration) and dissolved inorganic carbon (measured by coulometry) using CO2SYS [27]. (Online version in colour.)

Figure 2.

Echinoplutei from tropical, temperate and polar sea urchins reared in control and acidification treatments are smaller, and in some cases asymmetrical with arms differing markedly in length. All species were reared following similar methods [42,43,48,58]. Scale bars, 200 µm.

Figure 3.

Early echinopluteus of Tripneustes gratilla (Linneaus, 1758) in polarized light showing the postoral skeletal rod (between the arrows), supporting the arm. Scale bar, 100 µm. (Online version in colour.)

Figure 4.

Reduced growth of the postoral arm in echinoplutei in response to changes in (a) pH_NIST (National Institute of Standards and Technology) and (b) pCO₂ (log₁₀ transformed). The solid line is the regression line and the shaded area is 95% CI. Regression parameters are given in the electronic supplementary material, table S1. Different colours represent geographical regions (see legend). Percentage growth reduction (natural log transformed for curve fits) was back transformed for graphic representation.

Figure 5.

Reduced growth of the postoral arm in echinoplutei in response to changes in calcite and aragonite saturation. The solid line is the regression line and the shaded area is 95% CI. Regression parameters are given in the electronic supplementary material, table S1. Different colours represent geographical regions (see legend). Percentage growth reduction (natural log transformed for curve fits) was back transformed for graphic representation.

Figure 6.

Effects of reduced seawater pH_NIST on larval skeleton surface features. (a,b) Evechinus chloroticus (Valenciennes, 1846) larva showing postoral arm and skeletal rod (in box) in the living larvae and isolated for scanning electron microscopy. (c,d) Scanning view of the surface of the postoral arm rod of E. chloroticus reared in ambient (pH 8.1) and reduced seawater pH (pH 7.7) conditions, the latter showing surface etching and abnormal deposition. (e,f) The postoral arm rod of Sterechinus neumayeri (Meissner, 1900) reared in ambient (pH 8.0) and reduced seawater pH (pH 7.5) conditions with no changes evident [49]. (Online version in colour.)

Figure 7.

Effects of simultaneous exposure to increased temperature and reduced seawater pH_NIST on length of the postoral arm skeleton in the larvae of the Antarctic sea urchin Sterechinus neumayeri. Increased temperature increased larval growth in low pH treatments (n = 12, with 30 larvae measured per replicate [58]). (Online version in colour.)