PH Variability Exacerbates Effects of Ocean Acidification on a Caribbean Crustose Coralline Alga

Maggie D Johnson,Andrew H Altieri,Lucia M Rodriguez Bravo,Nicholas F Varley,Shevonne E O’Connor

doi:10.3389/fmars.2019.00150

Abstract

Crustose coralline algae (CCA) are among the most sensitive marine taxa to the pH changes predicted with ocean acidification (OA). However, many CCA exist in habitats where diel cycles in pH can surpass near-future OA projections. The prevailing theory that natural variability increases the tolerance of calcifiers to OA has not been widely tested with tropical CCA. Here, we assess the response of the reef-building species Lithophyllum congestum to stable and variable pH treatments, including an ambient control (amb/stable). The amb/variable treatment simulated an ambient diel cycle in pH (7.65-7.95), OA/stable simulated constant low pH reflecting worst-case year 2100 predictions (7.7), and OA/variable combined diel cycling with lower mean pH (7.45-7.75). We monitored the effects of pH on total calcification rate and photophysiology (maximum quantum yield) over 16 weeks. To assess the potential for acclimatization, we also quantified calcification rates during the first (0-8 weeks) and second (8-16 weeks) halves of the experiment. Calcification rates were lower in all pH treatments relative to ambient controls and photophysiology was unaffected. At the end of the 16-week experiment, total calcification rates were similarly low in the amb/variable and OA/stable treatment (27-29%), whereas rates declined by double in the OA/variable treatment (60%). When comparing the first and second halves of the experiment, there was no acclimatization in stable treatments as calcification rates remained unchanged in both the amb/stable and OA/stable treatments. In contrast, calcification rates deteriorated between periods in the variable treatments: from a 16-47% reduction in the amb/variable treatment to a 49-79% reduction in the OA/variable treatment, relative to controls. Our findings provide compelling evidence that pH variability can heighten CCA sensitivity to reductions in pH. Moreover, the decline in calcification rate over time directly contrasts prevailing theory that variability inherently increases organismal tolerances to low pH, and suggests that mechanisms of tolerance may become limited with increasing time of exposure. The significant role of diel pH cycling in CCA responses to OA indicates that organisms in habitats with diel variability could respond more severely to rapid changes in ocean pH associated with OA than predicted by experiments conducted under static conditions.

Highlights

Ocean acidification (OA) is a leading global threat to the persistence of coral reefs and other calcifier-dominated marine habitats (Hoegh-Guldberg et al, 2007)
This study found that variability superimposed on OA had no negative effects on net calcification in the tropical coralline Hydrolithon reinboldii, despite the increased time spent at extreme low pH
In contrast to the calcification response, photophysiology was unaffected by pH treatment, which indicates that the effects of pH treatment on calcification were independent of photosynthetic processes

Summary

Introduction

Ocean acidification (OA) is a leading global threat to the persistence of coral reefs and other calcifier-dominated marine habitats (Hoegh-Guldberg et al, 2007). In situ pH manipulations, such as free ocean carbon enrichment (FOCE) experiments (Kline et al, 2012) and studies using natural gradients in pH (e.g., CO2 vents and tide pools), have shed light the potential for natural variability to influence organismal and community-scale responses to pH reductions (Kroeker et al, 2013; Noisette et al, 2013; Stark et al, 2019) These experiments demonstrate how pH variability can influence the structure and trajectory of calcifier-dominated ecosystems (Kroeker et al, 2013) and can mediate the response of calcifiers to changes in mean pH (Georgiou et al, 2015). Applying this approach to manipulative experiments, by incorporating localscale pH variability into pH treatments, is a necessary step toward improving the predictive power and ecological relevance of laboratory perturbation experiments to nearshore ecosystems (Rivest et al, 2017; Vargas et al, 2017)

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