ReviewTwo decades of seawater acidification experiments on tropical scleractinian corals: Overview, meta-analysis and perspectives
Introduction
Due to the increasing emissions of carbon dioxide into the atmosphere, the Ocean is warming and getting more acidic. Ocean acidification (OA) has been identified as a global environmental threat and included as the United Nations' Sustainable Development Goal 14.3, as well as one of the nine planetary boundaries (Jagers et al. 2019; Rockström et al., 2009). OA impacts on marine species and ecosystems are well documented, including effect on marine calcifiers, threatening coral reefs as well as broader marine ecosystems (Doney et al., 2009; Feely, 2004; Gattuso and Hansson, 2011; Hendriks et al., 2010; Jiang et al., 2019; Kroeker et al., 2010, Kroeker et al., 2013; Orr et al., 2005).
Most of the available knowledge on the effects of OA on marine organisms comes from short-term laboratory experiments on isolated organisms (Kroeker et al., 2010). Fixed-term studies have the disadvantage of potentially under/overestimate the effects of OA, as some taxa may show vulnerability/acclimatization in the long-term (Fantazzini et al., 2015). Similarly, other life stages than those considered may show different vulnerability and controlled conditions does not consider the indirect effects due to OA-driven ecological changes (Fabricius et al., 2011). In this context, knowledge acquired through field experiments taking advantage of organisms that are naturally exposed to OA (e.g. CO2 vent systems) are very complementary as they account for the life-long acclimatization of organisms. These studies already showed that OA may change reef community composition and metabolism (Biscéré et al., 2019; Noonan et al., 2018). They also reported effects on skeletal porosity (Prada et al., 2021) and a variety of responses to OA on calcification rate, suggesting species-specific acclimatization to OA (Strahl et al., 2015).
Coral reefs have received particular attention as they are among the most severely threatened ecosystem on Earth (Pandolfi, 2003; Raven, 2005). The effects of seawater acidification on corals have been extensively studied (Chan and Connolly, 2013; Erez et al., 2011), but responses often differ between studies depending on parameters such as tested populations, species and life-cycle stages (Kawahata et al., 2019). These apparent conflicting results in the literature could also be attributed to variations in experimental designs and methodologies. In this study, we reviewed the literature that examined the effects of decreased pH on tropical scleractinian corals under laboratory-controlled conditions. A meta-analysis based on 169 experiments conducted in 141 peer-reviewed articles published since 1999 was performed, with four main objectives:
- (1)
To provide a semi-quantitative description of the evolution of research efforts testing the effects of seawater acidification on tropical scleractinian corals,
- (2)
To evaluate the effect of seawater acidification on coral biological functions,
- (3)
To investigate the modulating influence of exposure duration, coral life stages and coral genera on sensitivity to seawater acidification and,
- (4)
To highlight research gaps and bias.
Based on this review, we provide recommendations and perspectives for future research and an updated baseline for scientists starting in this field of research.
Section snippets
Material and methods
The code used in this manuscript was based on Jacob et al. (2020): https://doi.org/10.5281/zenodo.3694955.
Literature trend
In our database, we identified 169 experiments in 141 articles (listed in Supplementary material) that have evaluated the effects seawater acidification under laboratory-controlled conditions on tropical scleractinian corals. The six best studied regions account for 69% of the studies: Australia (15%), Japan (14%), French Polynesia (14%), Hawaii (10%), the USA (excluding Hawaii, 8%) and Taiwan (8%; Fig. 2A). Six percent of the studies were carried out on corals that have been maintained and
Research gaps and perspectives
Based on all aforementioned points, we selected a list of priorities and actions that should be addressed for future experimental works investigating the effects of seawater acidification on tropical scleractinians (Table 3).
Funding
This work was supported by the “Fondation de France” for a project called “ACID REEFS”, by the “Ministère de la Transition Ecologique et Solidaire” and the Foundation for Research on Biodiversity (FRB) for a project entitled “ACID REEFS2”.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We thank Jacob et al. (2020) for making their R scripts available and Dr. Moreau C. for his help in making Fig. 1. This work was funded by the Fondation de France for a project called “ACID REEFS”, by Ministère de la Transition écologique et Solidaire and the Foundation for Research on Biodiversity (FRB) for a project entitled “ACID REEFS”. The IAEA is grateful for the support provided to its Environment Laboratories by the Government of the Principality of Monaco.
References (166)
- et al.
The effects of thermal and high-CO2 stresses on the metabolism and surrounding microenvironment of the coral Galaxea fascicularis
C. R. Biol.
(2013) - et al.
A corrosive concoction: the combined effects of ocean warming and acidification on the early growth of a stony coral are multiplicative
J. Exp. Mar. Biol. Ecol.
(2011) - et al.
Mechanisms and thresholds for pH tolerance in Palau corals
J. Exp. Mar. Biol. Ecol.
(2017) - et al.
Physiological responses of corals to ocean acidification and copper exposure
Mar. Pollut. Bull.
(2018) - et al.
Effects of irradiance on the response of the coral Acropora pulchra and the calcifying alga Hydrolithon reinboldii to temperature elevation and ocean acidification
J. Exp. Mar. Biol. Ecol.
(2014) - et al.
Effects of exposure duration on the response of Pocillopora damicornis larvae to elevated temperature and high pCO2
J. Exp. Mar. Biol. Ecol.
(2013) The measurement of seawater pH
Mar. Chem.
(1993)- et al.
Vulnerability of marine biodiversity to ocean acidification: a meta-analysis
Estuar. Coast. Shelf Sci.
(2010) The reef coral two compartment proton flux model: a new approach relating tissue-level physiological processes to gross corallum morphology
J. Exp. Mar. Biol. Ecol.
(2011)- et al.
Reversal of ocean acidification enhances net coral reef calcification
Nature
(2016)
Projected near-future levels of temperature and pCO2 reduce coral fertilization success
PLoS ONE
Ocean acidification compromises recruitment success of the threatened Caribbean coral Acropora palmata
Proc. Natl. Acad. Sci.
Carbon dioxide addition to coral reef waters suppresses net community calcification
Nature
Parental effects improve escape performance of juvenile reef fish in a high-CO2 world
Proc. R. Soc. B Biol. Sci.
Independent effects of ocean warming versus acidification on the growth, survivorship and physiology of two acropora corals
Coral Reefs
Ocean acidification causes bleaching and productivity loss in coral reef builders
Proc. Natl. Acad. Sci.
Designating spatial priorities for marine biodiversity conservation in the coral triangle
Front. Mar. Sci.
Relative sensitivity of five Hawaiian coral species to high temperature under high-pCO2 conditions
Coral Reefs
Changes in coral reef communities across a natural gradient in seawater pH
Sci. Adv.
Coral host cells acidify symbiotic algal microenvironment to promote photosynthesis
Proc. Natl. Acad. Sci.
Rapid acclimation ability mediated by transcriptome changes in reef-building corals
Genome Biol. Evol.
The role of in hospite zooxanthellae photophysiology and reef chemistry on elevated pCO2 effects in two branching Caribbean corals: Acropora cervicornis and Porites divaricata
ICES J. Mar. Sci.
Coral thermal tolerance: tuning gene expression to resist thermal stress
PLoS ONE
Resistance to thermal stress in corals without changes in symbiont composition
Proc. R. Soc. B Biol. Sci.
Developmental carry over effects of ocean warming and acidification in corals from a potential climate refugium, Gulf of Aqaba
J. Exp. Biol.
High pCO2 promotes coral primary production
Biol. Lett.
Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs
Coral Reefs
Common Caribbean corals exhibit highly variable responses to future acidification and warming
Proc. R. Soc. B Biol. Sci.
Responses of coral gastrovascular cavity pH during light and dark incubations to reduced seawater pH suggest species-specific responses to the effects of ocean acidification on calcification
Coral Reefs
Differential effects of ocean acidification on growth and photosynthesis among phylotypes of symbiodinium (Dinophyceae)
Limnol. Oceanogr.
Presence of competitors influences photosynthesis, but not growth, of the hard coral Porites cylindrica at elevated seawater CO2
ICES J. Mar. Sci.
Differences in the responses of three scleractinians and the hydrocoral Millepora platyphylla to ocean acidification
Mar. Biol.
Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean
Oceanogr. Mar. Sci.
Reef-building corals thrive within hot-acidified and deoxygenated waters
Sci. Rep.
Low and variable pH decreases recruitment efficiency in populations of a temperate coral naturally present at a CO2 vent
Limnol. Oceanogr.
The reef-building coral Siderastrea siderea exhibits parabolic responses to ocean acidification and warming
Proc. R. Soc. B Biol. Sci.
Sensitivity of coral calcification to ocean acidification: a meta-analysis
Glob. Chang. Biol.
Is the response of coral calcification to seawater acidification related to nutrient loading?
Coral Reefs
Near-future reductions in pH will have no consistent ecological effects on the early life-history stages of reef corals
Mar. Ecol. Prog. Ser.
Geochemical perspectives on coral mineralization
Rev. Mineral. Geochem.
Effects of feeding and light intensity on the response of the coral Porites Rus to ocean acidification
Mar. Biol.
Water flow modulates the response of coral reef communities to ocean acidification
Sci. Rep.
The responses of eight coral reef calcifiers to increasing partial pressure of CO2 do not exhibit a tipping point
Limnol. Oceanogr.
Fast coral reef calcifiers are more sensitive to ocean acidification in short-term laboratory incubations
Limnol. Oceanogr.
The effect of ocean acidification on symbiont photorespiration and productivity in Acropora Formosa
Glob. Chang. Biol.
Reduced calcification and lack of acclimatization by coral colonies growing in areas of persistent natural acidification
Proc. Natl. Acad. Sci.
Calcifying coral abundance near low-pH springs: implications for future ocean acidification
Coral Reefs
Diel temperature and pH variability scale with depth across diverse coral reef habitats
Limnol. Oceanogr. Lett.
Impacts of climate warming on terrestrial ectotherms across latitude
Proc. Natl. Acad. Sci.
Guide to Best Practices for Ocean CO2 Measurements
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2023, Science of the Total EnvironmentCitation Excerpt :As atmospheric CO2 dissolves in seawater, it participates in a series of chemical reactions resulting in an increase of hydrogen ions concentration and, hence, a decrease in seawater pH (Pelejero et al., 2010; Doney et al., 2020). This also leads to a reduction of carbonate ions which are used by calcifying organisms to build their calcium carbonate shells or skeletons, making the calcification more difficult and the solid structures more vulnerable (Movilla et al., 2014; Doney et al., 2020; Godefroid et al., 2022). Together with other detrimental effects, ocean acidification is affecting marine ecosystems and biodiversity in different ways (Doney et al., 2020).