Sophie J. McCoy

Coralline algae (Rhodophyta) in a changing world: integrating ecological, physiological, and geochemical responses to global change.

Coralline algae are globally distributed benthic primary producers that secrete calcium carbonate skeletons. In the context of ocean acidification, they have received much recent attention due to the potential vulnerability of their high‐Mg calcite skeletons and their many important ecological roles. Herein, we summarize what is known about coralline algal ecology and physiology, providing context to understand their responses to global climate change. We review the impacts of these changes, including ocean acidification, rising temperatures, and pollution, on coralline algal growth and calcification. We also assess the ongoing use of coralline algae as marine climate proxies via calibration of skeletal morphology and geochemistry to environmental conditions. Finally, we indicate critical gaps in our understanding of coralline algal calcification and physiology and highlight key areas for future research. These include analytical areas that recently have become more accessible, such as resolving phylogenetic relationships at all taxonomic ranks, elucidating the genes regulating algal photosynthesis and calcification, and calibrating skeletal geochemical metrics, as well as research directions that are broadly applicable to global change ecology, such as the importance of community‐scale and long‐term experiments in stress response.

Historical comparisons reveal altered competitive interactions in a guild of crustose coralline algae

As the ocean environment changes over time, a paucity of long-term data sets and historical comparisons limits the exploration of community dynamics over time in natural systems. Here, we used a long-term experimental data set to present evidence for a reversal of competitive dominance within a group of crustose coralline algae (CCA) from the 1980s to present time in the northeast Pacific Ocean. CCA are cosmopolitan species distributed globally, and dominant space holders in intertidal and subtidal systems. Competition experiments showed a markedly lower competitive ability of the previous competitively dominant species and a decreased response of competitive dynamics to grazer presence. Competitive networks obtained from survey data showed concordance between the 1980s and 2013, yet also revealed reductions in interaction strengths across the assemblage. We discuss the potential role of environmental change, including ocean acidification, in altered ecological dynamics in this system.

Rapid Environmental Change over the Past Decade Revealed by Isotopic Analysis of the California Mussel in the Northeast Pacific

The anthropogenic input of fossil fuel carbon into the atmosphere results in increased carbon dioxide (CO2) into the oceans, a process that lowers seawater pH, decreases alkalinity and can inhibit the production of shell material. Corrosive water has recently been documented in the northeast Pacific, along with a rapid decline in seawater pH over the past decade. A lack of instrumentation prior to the 1990s means that we have no indication whether these carbon cycle changes have precedence or are a response to recent anthropogenic CO2 inputs. We analyzed stable carbon and oxygen isotopes (δ13C, δ18O) of decade-old California mussel shells (Mytilus californianus) in the context of an instrumental seawater record of the same length. We further compared modern shells to shells from 1000 to 1340 years BP and from the 1960s to the present and show declines in the δ13C of modern shells that have no historical precedent. Our finding of decline in another shelled mollusk (limpet) and our extensive environmental data show that these δ13C declines are unexplained by changes to the coastal food web, upwelling regime, or local circulation. Our observed decline in shell δ13C parallels other signs of rapid changes to the nearshore carbon cycle in the Pacific, including a decline in pH that is an order of magnitude greater than predicted by an equilibrium response to rising atmospheric CO2, the presence of low pH water throughout the region, and a record of a similarly steep decline in δ13C in algae in the Gulf of Alaska. These unprecedented changes and the lack of a clear causal variable underscores the need for better quantifying carbon dynamics in nearshore environments.

Morphology of the crustose coralline alga Pseudolithophyllum muricatum (Corallinales, Rhodophyta) responds to 30 years of ocean acidification in the Northeast Pacific

As the process of ocean acidification alters seawater carbon chemistry, physiological processes such as skeletal accretion are expected to become more difficult for calcifying organisms. The crustose coralline red algae (Corallinales, Rhodophyta) form an important guild of calcifying primary producers in the temperate Northeast Pacific. The morphology of important ecological traits, namely, skeletal density and thallus thickness near the growing edge, was evaluated in Pseudolithophyllum muricatum (Foslie) Steneck & R.T. Paine, the competitively dominant alga within this guild. P. muricatum shows a morphological response to increased ocean acidification in the temperate Northeast Pacific. Comparing historical (1981–1997) and modern (2012) samples from the field, crust thickness near the growing edge was approximately half as thick in modern samples compared with historical samples, while crust calcite density showed no significant change between the two sample groups. Morphological changes at the growing edge have important consequences for mediating competitive interactions within this guild of algae, and may affect the role of crustose coralline algal beds as hosts to infaunal communities and facilitators of recruitment in many invertebrate and macroalgal species.

Historical baselines and the future of shell calcification for a foundation species in a changing ocean

Seawater pH and the availability of carbonate ions are decreasing due to anthropogenic carbon dioxide emissions, posing challenges for calcifying marine species. Marine mussels are of particular concern given their role as foundation species worldwide. Here, we document shell growth and calcification patterns in Mytilus californianus, the California mussel, over millennial and decadal scales. By comparing shell thickness across the largest modern shells, the largest mussels collected in the 1960s–1970s and shells from two Native American midden sites (∼1000–2420 years BP), we found that modern shells are thinner overall, thinner per age category and thinner per unit length. Thus, the largest individuals of this species are calcifying less now than in the past. Comparisons of shell thickness in smaller individuals over the past 10–40 years, however, do not show significant shell thinning. Given our sampling strategy, these results are unlikely to simply reflect within-site variability or preservation effects. Review of environmental and biotic drivers known to affect shell calcification suggests declining ocean pH as a likely explanation for the observed shell thinning. Further future decreases in shell thickness could have significant negative impacts on M. californianus survival and, in turn, negatively impact the species-rich complex that occupies mussel beds.

Ocean acidification affects competition for space: projections of community structure using cellular automata.

Historical ecological datasets from a coastal marine community of crustose coralline algae (CCA) enabled the documentation of ecological changes in this community over 30 years in the Northeast Pacific. Data on competitive interactions obtained from field surveys showed concordance between the 1980s and 2013, yet also revealed a reduction in how strongly species interact. Here, we extend these empirical findings with a cellular automaton model to forecast ecological dynamics. Our model suggests the emergence of a new dominant competitor in a global change scenario, with a reduced role of herbivory pressure, or trophic control, in regulating competition among CCA. Ocean acidification, due to its energetic demands, may now instead play this role in mediating competitive interactions and thereby promote species diversity within this guild.

Coralline algal skeletal mineralogy affects grazer impacts

In macroalgal-dominated systems, herbivory is a major driver in controlling ecosystem structure. However, the role of altered plant-herbivore interactions and effects of changes to trophic control under global change are poorly understood. This is because both macroalgae and grazers themselves may be affected by global change, making changes in plant-herbivore interactions hard to predict. Coralline algae lay down a calcium carbonate skeleton, which serves as protection from grazing and is preserved in archival samples. Here, we compare grazing damage and intensity to coralline algae in situ over 4 decades characterized by changing seawater acidity. While grazing intensity, herbivore abundance and identity remained constant over time, grazing wound width increased together with Mg content of the skeleton and variability in its mineral organization. In one species, decreases in skeletal organization were found concurrent with deeper skeletal damage by grazers over time since the 1980s. Thus, in a future characterized by acidification, we suggest coralline algae may be more prone to grazing damage, mediated by effects of variability between individuals and species.

Physiological and Behavioral Plasticity of the Sea Cucumber Holothuria forskali (Echinodermata, Holothuroidea) to Acidified Seawater

Research into the effects of reduced pH caused by rising CO2 on echinoderms has been strongly biased toward those groups which rely heavily on calcification, such as sea urchins. There is very limited information available for groups that are less reliant on calcification, such as sea cucumbers. Moreover, plasticity in physiology and behavior in holothurians, which is considered to be critical to cope with ocean acidification, remains even less understood. Here, we examined the effects of a 22-week exposure to three pH levels (pH 7.97, 7.88, and 7.79) on the responses of adult Holothuria forskali. This is an abundant and ecologically important sea cucumber in shallow waters of the northeast Atlantic and Mediterranean. The holothurians did not exhibit serious acidosis after a 4-week gradually decreased pH exposure, possibly due to the slow acclimation period. After an additional 18 weeks of exposure, coelomic acid–base parameters did not differ significantly among the pH treatments, whereas they were higher than in week 4. Gonad development, defense behavior, and the structure and Ca2+ and Mg2+ concentrations of calcareous endoskeleton deposited in the body wall were all unaffected by decreased levels of seawater pH. No statistical differences were found after 22 weeks, and adult H. forskali showed strong physiological and behavioral plasticity to the effects of lowered seawater pH. While the interpretation of our results is restricted due to small sample sizes, this first long-term study of the effects of seawater acidification on sea cucumbers revealed resilience within the wide natural range of pCO2 found in NE Atlantic coastal waters.