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Direct and latent effects of ocean acidification on the transition of a sea urchin from planktonic larva to benthic juvenile.
Dorey N
,
Butera E
,
Espinel-Velasco N
,
Dupont S
.
Abstract
Ongoing ocean acidification is expected to affect marine organisms and ecosystems. While sea urchins can tolerate a wide range of pH, this comes at a high energetic cost, and early life stages are particularly vulnerable. Information on how ocean acidification affects transitions between life-history stages is scarce. We evaluated the direct and indirect effects of pH (pHT 8.0, 7.6 and 7.2) on the development and transition between life-history stages of the sea urchin Strongylocentrotus droebachiensis, from fertilization to early juvenile. Continuous exposure to low pH negatively affected larval mortality and growth. At pH 7.2, formation of the rudiment (the primordial juvenile) was delayed by two days. Larvae raised at pH 8.0 and transferred to 7.2 after competency had mortality rates five to six times lower than those kept at 8.0, indicating that pH also has a direct effect on older, competent larvae. Latent effects were visible on the larvae raised at pH 7.6: they were more successful in settling (45% at day 40 post-fertilization) and metamorphosing (30%) than larvae raised at 8.0 (17 and 1% respectively). These direct and indirect effects of ocean acidification on settlement and metamorphosis have important implications for population survival.
Figure 1. (A) Timeline of the experiment. The experiment started (Day post-fertilization, Dpf 0) with cleaving embryos that were distributed into five replicate jars at three different pHs (8.0, 7.6 and 7.2). At Dpf 29, larvae from three of the five replicate jars were distributed individually into wells inside three 24-well plates per new pH condition (i.e., n = 72 larvae for each treatment). (B) Experimental design: Two parameters were tested: (i) pH experienced by larvae (Dpf 1 to 29) and (ii) pH experienced by stages from competent larvae to juveniles (Dpf 30–40). Seven combinations were tested allowing to test three different hypotheses: (H1), continuous exposure to low pH throughout the development has a negative effect on larval, competent, newly settled and early juvenile development; (H2), low pH experienced by competent larvae have a direct negative effect on the settlement and metamorphosis success; and, (H3), settling individuals and metamorphosed juveniles from larvae raised under low pH are impaired relative to the ones raised under pH 8.0 (i.e., latent effect). (C) The Gompertz model used for settlement, with three descriptive parameters: maximum cumulated settlement (A; % larvae), maximum settlement rate (M; % larvae day-1) and initial latency period (λ; days from Dpf 30).
Figure 2. Effect of the pH treatments on the larval development (Dpf 1–29, H1): (A) mortality rates (% larvae µmBL–1), (B) body growth rates (µmBL day–1) and (C) rudiment size (μm; mean ± SD, vs. days post-fertilization); stars represent the significance of the pH effect (KW test; ** for p-value < 0.01, *** for p-value < 0.001; n = 5 replicates per pH treatment). (D) Rudiment size was significantly correlated to larval body size.
Figure 3. Effect of the combination of pH treatments on the settlement experiment (Dpf 29–40): At Dpf 29, individuals from three pH (“pH
experienced
by
larvae”, vertical pHs) were distributed in one of three pH treatments (horizontal pHs, see Fig. 1B). Full data points represent proportions calculated on the three well-plates combined (n = 72), while light grey data points are calculated in each of the well-plates (n = 24). (A) Mortality rates (mo, % indiv. day–1) were calculated as the linear relationship between survival (individuals alive, %) and days. (B) Settlement success (%) were fitted with Gompertz models (see Fig. 1B). A is the maximum cumulated settlement (% larvae), M is the maximum settlement rate (% larvae day–1) and λ is the initial latency period (days). Results of the models are detailed in Table 1. (C) Distribution of the newly metamorphosed individuals by body diameter at metamorphosis (μm). D represents the mean time (± SD) to metamorphosis (Dpf).
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