Maintained larval growth in mussel larvae exposed to acidified under-saturated seawater

Abstract

Ocean acidification (OA) is known to affect bivalve early life-stages. We tested responses of blue mussel larvae to a wide range of pH in order to identify their tolerance threshold. Our results confirmed that decreasing seawater pH and decreasing saturation state increases larval mortality rate and the percentage of abnormally developing larvae. Virtually no larvae reared at average pHT 7.16 were able to feed or reach the D-shell stage and their development appeared to be arrested at the trochophore stage. However larvae were capable of reaching the D-shell stage under milder acidification (pHT ≈ 7.35, 7.6, 7.85) including in under-saturated seawater with Ωa as low as 0.54 ± 0.01 (mean ± s. e. m.), with a tipping point for normal development identified at pHT 7.765. Additionally growth rate of normally developing larvae was not affected by lower pHT despite potential increased energy costs associated with compensatory calcification in response to increased shell dissolution. Overall, our results on OA impacts on mussel larvae suggest an average pHT of 7.16 is beyond their physiological tolerance threshold and indicate a shift in energy allocation towards growth in some individuals revealing potential OA resilience.

Figure 1. Decreasing mortality, abnormality and maintained growth rates with increasing pH.

(a) Relationship between larval mortality rates (ln (relative density) ln (day)⁻¹) and average pH_T. Mortality rates for each point correspond to the regression slope coefficients extracted from significant power relationships between relative density and time (day). For clarity y axis values have been converted to positive values. (b) Relationship between the percentage of larval abnormality and average pH_T. (c) Relationship between growth rate (μm day⁻¹) of normally D-shaped larvae and average pH_T. Growth rates for each point correspond to the regression slope coefficients extracted from significant Theil-Sen median based linear relationships between mean larval length (μm) and time (day).

Figure 2. Most common larval phenotypes observed throughout the course of the experiment.

(a) Trochophore stage, (b) protruding mantle, (c) indented margin, (d) convex hinge, (e) cupped and (f) normally D-shaped larva. N. B. All photos are from experiment day 11.

Figure 3. Lower feeding rates at nominal pH 7.1.

Mean % ± s.e.m. feeding rates (ng C ind⁻¹h⁻¹) in M. edulis D-shaped larvae cultured at 5 different nominal pHs.

Figure 4. Quantification of calcification and dissolution using calcein.

Confocal image of calcein-labelled skeleton of 11 day old D-shaped larvae of M. edulis cultured for 2 days in green calcein (d1-2, green signal) at either pH 8.1 or pH 7.0 and then transferred for 2 days in blue calcein (d3-4, red signal). Larvae exposed to pH 7.0 at days 3–4 have a larger red band revealing increased calcification as well as less green signal suggesting higher dissolution.

Figure 5. Higher calcification and shell dissolution at lower pH.

Mean % ± s.e.m. relative calcification (%; (a,b)) and dissolution (%, (c)) in M. edulis 11 days old D-shaped larvae exposed to a 2 days treatment at pH 8.1 or pH 7.0 (a), then transferred to either the same (pH 8.1–8.1 and pH 7.0–7.0) or the other (pH 8.1–7.0 and pH 7.0–8.1) for 2 more days (b,c).