Umeå University's logo

Linguistic uncertainty is a prime source of uncertainty pervading ecology and conservation. Coralline algae are a widespread and diverse group of calcifying red macroalgae that underpin coastal ecosystem function and service provision. Recent increasing interest in coralline algae in the scientific literature has revealed a diverse but confusing terminology at organism to habitat scales. Coralline algal research and conservation are international and multidisciplinary, so there are geographic and disciplinary imbalances in research and conservation efforts. To reach consensus and reduce uncertainty, we propose a unified terminology. We review trends in cultural and scientific use of coralline algal terms and propose a system based on six morphologies: (1) attached, (2) free-living geniculate, (3) encrusting and free-living nongeniculate coralline algae, the latter either being (4) nucleated or (5) non-nucleated thalli or (6) fragments. We take inspiration from other coastal systems that have achieved consensus through umbrella terms, such as ‘coral’ and ‘kelp’, to accelerate global progress in coralline algal research and conservation. We characterise 14 coralline algae–dominated habitat global types, falling within seven functional groups, four biomes and four realms: (1) freshwater coralline streams; (2) coralline tide pools; (3) intertidal coralline rims and (4) turf; (5) coralline sea caves; (6) coral–algal reefs; (7) algal ridges; (8) coralligenous reefs; subtidal (9) carbonate crusts, (10) coralline barrens and (11) turf; and (12) articulith, (13) maerl and (14) rhodolith beds, which fall into the coralline algal bed functional group. We hope this unified terminology promotes data comparison, enables cross-boundary and cross-sector sharing of best practices, develops capacity for meta-analyses and improves conservation strategies.

The increasing severity and frequency of mass bleaching events has placed shallow-water tropical coral reefs at risk of significant decline in the coming decades. The association of endosymbiotic dinoflagellates (Family: Symbiodiniaceae) with corals is regulated by local environmental conditions along with evolutionary history and plays a leading role in bleaching sensitivity and recovery. Resolving temporal and spatial dynamics of coral-Symbiodiniaceae associations is therefore essential for accurate bleaching risk predictions. Here, we investigated temporal patterns in dominant Symbiodiniaceae across the Greater Caribbean region, which is heavily impacted by human activities, disease and climate change. Using records derived from genetic databases, we considered Symbiodiniaceae dominance from 1994 to 2009, with a particular focus on and around the 2005 mass bleaching event. From the 4 Symbiodiniaceae genera recorded (Symbiodinium, Breviolum, Cladocopium and Durusdinium spp.), we identified genera-specific responses to ocean heating and bleaching stress. Generalist symbiont representatives were dominant only during periods of sustained environmental stability. In contrast, during and immediately after bleaching saw the emergence and subsequent persistence of Durusdinium spp.—an invasive genus in the Caribbean with high thermal tolerance but which induces negative impacts on coral physiology and calcification. In post-bleaching recovery years, a regional-scale bet-hedging strategy was adopted allowing thermal tolerance to be maintained, but poised for a more physiologically beneficial symbiosis if/when environmental conditions become favourable. Our regional-scale, multi-year perspective gives support for local-/colony-scale tuning of coral-Symbiodiniaceae relationships, and highlights how continued warming and bleaching stress will enable Durusdinium spp. invasion to persist, with knock-on implications for future coral reef development.

The extent of projected ocean acidification is partly dependent on the natural variability of marine carbonate chemistry—which is higher in coastal systems than in the open ocean. However, there are limited empirical studies quantifying the rate, magnitude and drivers of coastal environmental variability, preventing accurate assessments for how species and their associated communities may respond to projected climate change. Here, we quantified the annual variability of pH, temperature and dissolved oxygen in a coralline algae reef, a globally distributed biodiverse habitat that may be one of the most sensitive to projected climate change. We found that coralline algae and their communities are exposed to pH values as low as those projected for 2100 (even under a low emission scenario) for 63% of the year, including most of autumn and all of winter. Annual fluctuations in pH ranged by 0.46 units, with identifiable patterns at diel to seasonal timescales driven by various biogeochemical factors. Biologically driven patterns in dissolved oxygen and pH were coupled at multiple periodicities, and temperature was coupled to pH during the winter. Tidal cycling additionally modulated biological forcing of pH, increasing the complexity of intra-seasonal pH variability. Forecasting this environmental variability to the future led to projections of new pH extremes well beyond all IPCC emission scenarios. However, persistent long-term exposure to low pH may increase the acclimation and adaptation potential of coralline algae and their associated communities, providing a level of optimism for the continued survival of this habitat despite sensitivity to projected climate change.

Rhodolith beds are diverse and globally distributed habitats. Nonetheless, the role of rhodoliths in structuring the associated species community through a hierarchy of positive interactions is yet to be recognised. In this review, we provide evidence that rhodoliths can function as foundation species of multi-level facilitation cascades and, hence, are fundamental for the persistence of hierarchically structured communities within coastal oceans. Rhodoliths generate facilitation cascades by buffering physical stress, reducing consumer pressure and enhancing resource availability. Due to large variations in their shape, size and density, a single rhodolith bed can support multiple taxonomically distant and architecturally distinct habitat-forming species, such as primary producers, sponges or bivalves, thus encompassing a broad range of functional traits and providing a wealth of secondary microhabitat and food resources. In addition, rhodoliths are often mobile, and thus can redistribute associated species, potentially expanding the distribution of species with short-distance dispersal abilities. Key knowledge gaps we have identified include: the experimental assessment of the role of rhodoliths as basal facilitators; the length and temporal stability of facilitation cascades; variations in species interactions within cascades across environmental gradients; and the role of rhodolith beds as climate refugia. Addressing these research priorities will allow the development of evidence-based policy decisions and elevate rhodolith beds within marine conservation strategies.

Long-lived calcifying marine biota are increasingly used as paleo-archives for reconstructing ocean pH. They enable exploration of the rate and magnitude of ocean acidification in shallow-water ecosystems serving as proxies for environmental pH reconstruction. However, shallow water systems often have highly variable carbonate chemistry, and the impact of this on the accuracy of pH reconstructions from long-lived marine calcifiers is not known. In particular, a better understanding of the timing of calcification with respect to environmental pH cyclicity is needed. To test the fidelity of coastal environmental pH proxies, we assessed the synchronicity between calcification and in situ diel carbonate chemistry in a tropical (One Tree Island, Great Barrier Reef, Australia) and a temperate (Loch Sween, Scotland) location using calcifying macroalgae (rhodolith-forming coralline algae) as a model system. Calcification occurred primarily during daylight hours, meaning a recording bias was introduced when compared to the full diel pH range (< 0.02 pH units). This bias resulted in pH offsets up to 0.043 pH units over the period 1860-2020, representing up to 34% of the projected pH change from 1860 in the tropics and up to 1.8% in temperate latitudes. Therefore, when proxy records are used to extend modern instrumental records of pH, we find that this may lead to bias, indicating daytime, nighttime, and full diel pH records should be assessed separately. We suggest that temporal pH cycles should be characterized at a local scale to enable incorporation of potential biases in the application of calcifying marine macroalgae to reconstruct pH change.

Red coralline algae create abundant, spatially vast, reef ecosystems throughout our coastal oceans with significant ecosystem service provision, but our understanding of their basic physiology is lacking. In particular, the balance and linkages between carbon-producing and carbon-sequestering processes remain poorly constrained, with significant implications for understanding their role in carbon sequestration and storage. Using dual radioisotope tracing, we provide evidence for coupling between photosynthesis (which requires CO2) and calcification (which releases CO2) in the red coralline alga Boreolithothamnion soriferum (previously Lithothamnion soriferum)-a marine ecosystem engineer widely distributed across Atlantic mid-high latitudes. Of the sequestered HCO3-, 38 ± 22% was deposited as carbonate skeleton while 39 ± 14% was incorporated into organic matter via photosynthesis. Only 38 ± 2% of the sequestered HCO3- was transformed into CO2, and almost 40% of that was internally recycled as photosynthetic substrate, reducing the net release of carbon to 23 ± 3% of the total uptake. The calcification rate was strongly dependent on photosynthetic substrate production, supporting the presence of photosynthetically enhanced calcification. The efficient carbon-recycling physiology reported here suggests that calcifying algae may not contribute as much to marine CO2 release as is currently assumed, supporting a reassessment of their role in blue carbon accounting.

Ocean Acidification (OA) arises from the increase in atmospheric carbon dioxide concentration following the industrial revolution. The ecological and socio-economic consequences of OA were first identified around 10–15 years ago but remain poorly understood. This is particularly true in coastal regions where local processes can have dramatic consequences on pH trends through time, obscuring and compounding the long-term effects from rising atmospheric CO2. Here we explore the possibility of generating long records of coastal ocean pH using the skeletons of widely distributed coralline algae (CA). The skeletons of these slow growing (<1 mm/year) taxa often contain micron-scale heterogeneities, making sampling for high-resolution climate reconstructions using bulk sampling techniques difficult. Here we use laser ablation coupled to inductively coupled plasma mass spectrometers to generate high-resolution 2D images of the element/calcium ratios and boron isotope composition (δ11B) of a sample of Boreolithothamniom cf. soriferum from Loch Sween in Scotland, UK where we have been monitoring temperature since 2004 and pH during 2014. By carefully correlating the geochemical images with a scanning electron microscopy image we can segment them to remove the marginal portions of the skeleton, isolating the central growth axis to generate an age model and growth rate. The δ11B-pH is significantly elevated above the seawater pH in Loch Sween (8.4 to 8.9 vs. 7.9 to 8.1) consistent with other CA that show internal pH elevation. On a seasonal scale, internal pH is negatively correlated with temperature and also exhibits a long-term decline. By removing this temperature effect, internal pH can be correlated to seawater pH during the 2014 monitoring period allowing us to reconstruct a seawater acidification trend from 2004 to 2018 of -0.018 pH units per year, 10x higher than open ocean trends but consistent with contemporaneous monitoring efforts of UK coastal waters. Reconstructed aqueous CO2 suggests that prior to ∼2008 Loch Sween was a sink of CO2 but after this date, particularly during the early summer, it was a substantial CO2 source. Comparison of reconstructed aqueous CO2 with a record of calcification rate of our sample of Boreolithothamniom cf. soriferum suggests this acidification and associated rise in local seawater pCO2 may have freed this sample from carbon limitation leading to a recent increase in calcification.

Coral reefs provide ecosystem benefits to millions of people but are threatened by rapid environmental change and ever-increasing human pressures. Restoration is becoming a priority strategy for coral reef conservation, yet implementation remains challenging and it is becoming increasingly apparent that indirect conservation and restoration approaches will not ensure the long-term sustainability of coral reefs. The important role of environmental conditions in restoration practice are currently undervalued, carrying substantial implications for restoration success. Giving paramount importance to environmental conditions, particularly during the pre-restoration planning phase, has the potential to bring about considerable improvements in coral reef restoration and innovation. This Essay argues that restoration risk may be reduced by adopting an environmentally aware perspective that gives historical, contemporary, and future context to restoration decisions. Such an approach will open up new restoration opportunities with improved sustainability that have the capacity to dynamically respond to environmental trajectories.

Photoautotrophic marine ecosystems can lock up organic carbon in their biomass and the associated organic sediments they trap over millennia and are thus regarded as blue carbon ecosystems. Because of the ability of marine ecosystems to lock up organic carbon for millennia, blue carbon is receiving much attention within the United Nations' 2030 Agenda for Sustainable Development as a nature-based solution (NBS) to climate change, but classically still focuses on seagrass meadows, mangrove forests, and tidal marshes. However, other coastal ecosystems could also be important for blue carbon storage, but remain largely neglected in both carbon cycling budgets and NBS strategic planning. Using a meta-analysis of 253 research publications, we identify other coastal ecosystems—including mud flats, fjords, coralline algal (rhodolith) beds, and some components or coral reef systems—with a strong capacity to act as blue carbon sinks in certain situations. Features that promote blue carbon burial within these ‘non-classical’ blue carbon ecosystems included: (1) balancing of carbon release by calcification via carbon uptake at the individual and ecosystem levels; (2) high rates of allochthonous organic carbon supply because of high particle trapping capacity; (3) high rates of carbon preservation and low remineralization rates; and (4) location in depositional environments. Some of these features are context-dependent, meaning that these ecosystems were blue carbon sinks in some locations, but not others. Therefore, we provide a universal framework that can evaluate the likelihood of a given ecosystem to behave as a blue carbon sink for a given context. Overall, this paper seeks to encourage consideration of non-classical blue carbon ecosystems within NBS strategies, allowing more complete blue carbon accounting.