Ocean pH fluctuations affect mussel larvae at key developmental transitions.

L Kapsenberg,M C Bitter,E Tambutté,J.-P Gattuso,R Dumollard,A Miglioli

doi:10.1098/rspb.2018.2381

Abstract

Coastal marine ecosystems experience dynamic fluctuations in seawater carbonate chemistry. The importance of this variation in the context of ocean acidification requires knowing what aspect of variability biological processes respond to. We conducted four experiments (ranging from 3 to 22 days) with different variability regimes (pHT 7.4–8.1) assessing the impact of diel fluctuations in carbonate chemistry on the early development of the mussel Mytilus galloprovincialis. Larval shell growth was consistently correlated to mean exposures, regardless of variability regimes, indicating that calcification responds instantaneously to seawater chemistry. Larval development was impacted by timing of exposure, revealing sensitivity of two developmental processes: development of the shell field, and transition from the first to the second larval shell. Fluorescent staining revealed developmental delay of the shell field at low pH, and abnormal development thereof was correlated with hinge defects in D-veligers. This study shows, for the first time, that ocean acidification affects larval soft-tissue development, independent from calcification. Multiple developmental processes additively underpin the teratogenic effect of ocean acidification on bivalve larvae. These results explain why trochophores are the most sensitive life-history stage in marine bivalves and suggest that short-term variability in carbonate chemistry can impact early larval development.

Highlights

Coastal marine ecosystems experience dynamic spatio-temporal variability in seawater inorganic carbonate chemistry [1]
Subsequent shell growth is highly dependent on Va or SIR [23,24], due to the fact that larvae have limited control over carbonate chemistry at the site of calcification [25]. These findings suggest that early development of bivalves is comprised of process-specific sensitivities, and shortterm fluctuations in carbonate chemistry typical of shallow coastal waters may be important to larval development
By using a range of variability treatments, we show that shell growth responds to mean exposures while development depends on time-sensitive exposures (Exp. 1– 4), and these processes additively contribute to overall D-veliger phenotypes

Summary

Introduction

Coastal marine ecosystems experience dynamic spatio-temporal variability in seawater inorganic carbonate chemistry [1]. Short-term variability occurs on top of baseline changes associated with ocean acidification. Ocean acidification causes a decrease in mean seawater pH and aragonite saturation state (Va) via absorption of anthropogenic carbon dioxide (CO2) emissions [2]. How the interplay of acidification and coastal pH variability will impact marine organisms requires understanding what aspect of pH variability influences biological processes that occur over similar time frames [4,5]. Fluctuations in coastal carbonate chemistry often occur on a diel period. Diel fluctuations result from daytime photosynthetic removal of CO2 by phytoplankton and benthic photoautotrophs followed by night-time respiration of the whole community [6]. Seagrasses, macroalgae and kelp forests can induce diel pH fluctuations that span a few

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