Structural integrity and skeletal trace elements in intertidal coralline algae across the Northeast Atlantic reveal a distinct separation of the leading and the trailing edge populations.

Intertidal macroalgae, such as coralline algae, represent an essential structural element and substrate in rocky coastal zones. They have a high degree of flexibility allowing their survival in environments with severe mechanical stress during tidal cycles. This study characterised the genicula and intergenicula of the calcifying red algae Corallina officinalis across its geographic distribution in the Northeast Atlantic. Poleward populations have constructed more sturdy cell walls compared to equatorward populations, potentially due to greater local adaptations to higher frequency and intensity of environmental factors like storms and wave action. Southern populations showed a lack of local adaptation culminating in survival rather than thriving within their current environment, hence, they are located at the margin of this species' favourable conditions. Results clarify significant differences between latitudes and indicate a north-to-south gradient in this species' skeletal elemental composition. Northern populations were dominated by cadmium, whereas chromium was the major trace element found in southern populations. In the future, these characteristics could lead to a permanent decline and a decrease in the ecosystem functions of C. officinalis in the southern locations in the Northeast Atlantic, which may be accelerated by predicted future climatic changes.

Levelling-up rhodolith-bed science to address global-scale conservation challenges.

Global marine conservation remains fractured by an imbalance in research efforts and policy actions, limiting progression towards sustainability. Rhodolith beds represent a prime example, as they have ecological importance on a global scale, provide a wealth of ecosystem functions and services, including biodiversity provision and potential climate change mitigation, but remain disproportionately understudied, compared to other coastal ecosystems (tropical coral reefs, kelp forests, mangroves, seagrasses). Although rhodolith beds have gained some recognition, as important and sensitive habitats at national/regional levels during the last decade, there is still a notable lack of information and, consequently, specific conservation efforts. We argue that the lack of information about these habitats, and the significant ecosystem services they provide, is hindering the development of effective conservation measures and limiting wider marine conservation success. This is becoming a pressing issue, considering the multiple severe pressures and threats these habitats are exposed to (e.g., pollution, fishing activities, climate change), which may lead to an erosion of their ecological function and ecosystem services. By synthesizing the current knowledge, we provide arguments to highlight the importance and urgency of levelling-up research efforts focused on rhodolith beds, combating rhodolith bed degradation and avoiding the loss of associated biodiversity, thus ensuring the sustainability of future conservation programs.

An intertidal life: Combined effects of acidification and winter heatwaves on a coralline alga (Ellisolandia elongata) and its associated invertebrate community.

In coastal marine ecosystems coralline algae often create biogenic reefs. These calcareous algal reefs affect their associated invertebrate communities via diurnal oscillations in photosynthesis, respiration and calcification processes. Little is known about how these biogenic reefs function and how they will be affected by climate change. We investigated the winter response of a Mediterranean intertidal biogenic reef, Ellissolandia elongata exposed in the laboratory to reduced pH conditions (i.e. ambient pH - 0.3, RCP 8.5) together with an extreme heatwave event (+1.4 °C for 15 days). Response variables considered both the algal physiology (calcification and photosynthetic rates) and community structure of the associated invertebrates (at taxonomic and functional level). The combination of a reduced pH with a heatwave event caused Ellisolandia elongata to significantly increase photosynthetic activity. The high variability of calcification that occurred during simulated night time conditions, indicates that there is not a simple, linear relationship between these two and may indicate that it will be resilient to future conditions of climate change. In contrast, the associated fauna were particularly negatively affected by the heatwave event, which impoverished the communities as opportunistic taxa became dominant. Local increases in oxygen and pH driven by the algae can buffer the microhabitat in the algal fronds, thus favouring the survival of small invertebrates.

Structural and Elemental Analysis of the Freshwater, Low-Mg Calcite Coralline Alga Pneophyllum cetinaensis.

Coralline algae are one of the most diversified groups of red algae and represent a major component of marine benthic habitats from the poles to the tropics. This group was believed to be exclusively marine until 2016, when the first freshwater coralline algae Pneophyllum cetinaensis was discovered in the Cetina River, southern Croatia. While several studies investigated the element compositions of marine coralline algal thalli, no information is yet available for the freshwater species. Using XRD, LA-ICP-MS and nano indentation, this study presents the first living low-Mg calcite coralline algae with Mg concentrations ten times lower than is common for the average marine species. Despite the lower Mg concentrations, hardness and elastic modulus (1.71 ± 1.58 GPa and 29.7 ± 18.0 GPa, respectively) are in the same range as other marine coralline algae, possibly due to other biogenic impurities. When compared to marine species, Ba/Ca values were unusually low, even though Ba concentrations are generally higher in rivers than in seawater. These low values might be linked to different physical and chemical characteristics of the Cetina River.

Physiological response of the coralline alga Corallina officinalis L. to both predicted long-term increases in temperature and short-term heatwave events.

Climate change is leading to an increase of mean sea surface temperatures and extreme heat events. There is an urgent need to better understand the capabilities of marine macroalgae to adapt to these rapid changes. In this study, the responses of photosynthesis, respiration, and calcification to elevated temperature in a global warming scenario were investigated in the coralline alga Corallina officinalis. Algae were cultured for 7 weeks under 4 temperature treatments: (1) control under ambient-summer conditions (C, ~20 °C), (2) simulating a one-week heatwave of 1 °C (HW, Tcontrol+1 °C), (3) elevated temperature (+3, Tcontrol +3 °C), (4) combination of the two previous treatments (HW+3, T+3+1 °C). After exposure at T+3 (up to a Tmax of ~23 °C), respiration and photosynthesis increased significantly. After 5 weeks, calcification rates were higher at elevated temperatures (T+3 and THW+3) compared to Tcontrol, but at the end of the experiment (7 weeks) calcification decreased significantly at those temperatures beyond the thermal optimum (six-fold at T+3, and three-fold at THW+3, respectively). The same trend was noted for all the physiological processes, suggesting that a prolonged exposure to high temperatures (7 weeks up to T+3) negatively affect the physiology of C. officinalis, as a possible consequence of thermal stress. A one-week heatwave of +1 °C with respect to Tcontrol (at THW) did not affect respiration, photosynthesis, or calcification rates. Conversely, a heatwave of 1 °C, when combined with the 3 °C increase predicted by the end of the century (at THW+3), induced a reduction of physiological rates. Continued increases in both the intensity and frequency of heatwaves under anthropogenic climate change may lead to reduced growth and survival of primary producers such as C. officinalis.

The oceans are changing: impact of ocean warming and acidification on biofouling communities.

Climate change (CC) is driving modification of the chemical and physical properties of estuaries and oceans with profound consequences for species and ecosystems. Numerous studies investigate CC effects from species to ecosystem levels, but little is known of the impacts on biofilm communities and on bioactive molecules such as cues, adhesives and enzymes. CC is induced by anthropogenic activity increasing greenhouse emissions leading to rises in air and water temperatures, ocean acidification, sea level rise and changes in ocean gyres and rainfall patterns. These environmental changes are resulting in alterations within marine communities and changes in species ranges and composition. This review provides insights and synthesis of knowledge about the effect of elevated temperature and ocean acidification on microfouling communities and bioactive molecules. The existing studies suggest that CC will impact production of bioactive compounds as well as the growth and composition of biofouling communities. Undoubtedly, with CC fouling management will became an even greater challenge.

Understanding the margin squeeze: Differentiation in fitness-related traits between central and trailing edge populations of Corallina officinalis.

ABSTRACT: Assessing population responses to climate-related environmental change is key to understanding the adaptive potential of the species as a whole. Coralline algae are critical components of marine shallow water ecosystems where they function as important ecosystem engineers. Populations of the calcifying algae Corallina officinalis from the center (southern UK) and periphery (northern Spain) of the North Atlantic species natural distribution were selected to test for functional differentiation in thermal stress response. Physiological measurements of calcification, photosynthesis, respiration, growth rates, oxygen, and calcification evolution curves were performed using closed cell respirometry methods. Species identity was genetically confirmed via DNA barcoding. Through a common garden approach, we identified distinct vulnerability to thermal stress of central and peripheral populations. Southern populations showed a decrease in photosynthetic rate under environmental conditions of central locations, and central populations showed a decline in calcification rates under southern conditions. This shows that the two processes of calcification and photosynthesis are not as tightly coupled as previously assumed. How the species as whole will react to future climatic changes will be determined by the interplay of local environmental conditions and these distinct population adaptive traits. OPEN RESEARCH BADGES: This article has earned an Open Materials Badge for making publicly available the components of the research methodology needed to reproduce the reported procedure and analysis. All materials are available at https://doi.pangaea.de/10.1594/PANGAEA.899568.

Isolation and characterization of nine microsatellite markers for the red alga Corallina officinalis.

We report the development of nine polymorphic microsatellite markers for Corallina officinalis (Linnaeus, 1758), a calcifying intertidal red alga and important ecosystem engineer spread along the North East Atlantic. Characterization and analysis of loci were made using 15 individuals of C. officinalis from populations in Iceland and the UK. The average number of alleles per locus was 3.78 (range 2-6) and mean of gene diversity was 0.58 (range 0.38-0.77). The set of microsatellites developed here will provide a useful molecular tool for population genetic and conservation studies.

Elemental variability in the coralline alga Lithophyllum yemenense as an archive of past climate in the Gulf of Aden (NW Indian Ocean).

This study presents the first algal thallus (skeleton) archive of Asian monsoon strength and Red Sea influence in the Gulf of Aden. Mg/Ca, Li/Ca, and Ba/Ca were measured in Lithophyllum yemenense from Balhaf (Gulf of Aden) using laser ablation inductively coupled plasma mass spectrometry, and Mg/Ca ratio oscillation was used to reconstruct the chronology (34 y). Oscillations of element rates corresponding to the algal growth between 1974 and 2008 were compared with recorded climate and oceanographic variability. During this period, sea surface temperatures (SST) in Balhaf recorded a warming trend of 0.55°C, corresponding to an increase in Mg and Li content in the algal thallus of 2.1 mol-% and 1.87 µmol-%, respectively. Lithophyllum yemenense recorded decadal SST variability by Li/Ca, and the influence of the Pacific El-Niño Southern Oscillation on the NW Indian Ocean climate system by Ba/Ca. Additionally, algal Mg/Ca, Li/Ca, and Ba/Ca showed strong and significant correlations with All Indian Rainfall in the decadal range indicating that these proxies can be useful for tracking variability in the Indian monsoon system, possibly due to changes of the surface wind system, with deep water upwelling in summer, and a distinct seasonality.

Effects of thermal stress on the growth of an intertidal population of Ellisolandia elongata (Rhodophyta) from N-W Mediterranean Sea.

Coralline algae are calcareous algae able to build biogenic structures, thus playing a key-role as marine biodiversity promoters and calcium carbonate producers. The aim was to estimate the growth of Ellisolandia elongata under thermal stress. E. elongata were cultured for 2, 4 and 6 months under "natural" temperature (Tc) and increased temperature (Ti = Tc + 3 °C). In order to determine a possible culturing effect, growth in the field was also measured. For the first time, Alizarin Red S dye was used in high energy shallow water environments. Thallus linear extension was higher in the cultured specimens (Tc and Ti) compared to the field specimens. The carbonate mass in the field was higher than in Ti and Tc after 2, 4 months but decreased after 6 months. Partly unknown in situ environmental factors could have affected growth and calcification rates in the field while thermal adaptation could explain growth rates in the culturing experiment.

Century-scale trends and seasonality in pH and temperature for shallow zones of the Bering Sea.

No records exist to evaluate long-term pH dynamics in high-latitude oceans, which have the greatest probability of rapid acidification from anthropogenic CO2 emissions. We reconstructed both seasonal variability and anthropogenic change in seawater pH and temperature by using laser ablation high-resolution 2D images of stable boron isotopes (δ(11)B) on a long-lived coralline alga that grew continuously through the 20th century. Analyses focused on four multiannual growth segments. We show a long-term decline of 0.08 ± 0.01 pH units between the end of the 19th and 20th century, which is consistent with atmospheric CO2 records. Additionally, a strong seasonal cycle (∼ 0.22 pH units) is observed and interpreted as episodic annual pH increases caused by the consumption of CO2 during strong algal (kelp) growth in spring and summer. The rate of acidification intensifies from -0.006 ± 0.007 pH units per decade (between 1920s and 1960s) to -0.019 ± 0.009 pH units per decade (between 1960s and 1990s), and the episodic pH increases show a continuous shift to earlier times of the year throughout the centennial record. This is indicative of ecosystem shifts in shallow water algal productivity in this high-latitude habitat resulting from warming and acidification.

The future of the northeast Atlantic benthic flora in a high CO2 world.

Seaweed and seagrass communities in the northeast Atlantic have been profoundly impacted by humans, and the rate of change is accelerating rapidly due to runaway CO2 emissions and mounting pressures on coastlines associated with human population growth and increased consumption of finite resources. Here, we predict how rapid warming and acidification are likely to affect benthic flora and coastal ecosystems of the northeast Atlantic in this century, based on global evidence from the literature as interpreted by the collective knowledge of the authorship. We predict that warming will kill off kelp forests in the south and that ocean acidification will remove maerl habitat in the north. Seagrasses will proliferate, and associated epiphytes switch from calcified algae to diatoms and filamentous species. Invasive species will thrive in niches liberated by loss of native species and spread via exponential development of artificial marine structures. Combined impacts of seawater warming, ocean acidification, and increased storminess may replace structurally diverse seaweed canopies, with associated calcified and noncalcified flora, with simple habitats dominated by noncalcified, turf-forming seaweeds.

Phenotypic plasticity of coralline algae in a High CO2 world.

It is important to understand how marine calcifying organisms may acclimatize to ocean acidification to assess their survival over the coming century. We cultured the cold water coralline algae, Lithothamnion glaciale, under elevated pCO2 (408, 566, 770, and 1024 µatm) for 10 months. The results show that the cell (inter and intra) wall thickness is maintained, but there is a reduction in growth rate (linear extension) at all elevated pCO2. Furthermore a decrease in Mg content at the two highest CO2 treatments was observed. Comparison between our data and that at 3 months from the same long-term experiment shows that the acclimation differs over time since at 3 months, the samples cultured under high pCO2 showed a reduction in the cell (inter and intra) wall thickness but a maintained growth rate. This suggests a reallocation of the energy budget between 3 and 10 months and highlights the high degree plasticity that is present. This might provide a selective advantage in future high CO2 world.

Ocean acidification weakens the structural integrity of coralline algae.

The uptake of anthropogenic emission of carbon dioxide is resulting in a lowering of the carbonate saturation state and a drop in ocean pH. Understanding how marine calcifying organisms such as coralline algae may acclimatize to ocean acidification is important to understand their survival over the coming century. We present the first long-term perturbation experiment on the cold-water coralline algae, which are important marine calcifiers in the benthic ecosystems particularly at the higher latitudes. Lithothamnion glaciale, after three months incubation, continued to calcify even in undersaturated conditions with a significant trend towards lower growth rates with increasing pCO2 . However, the major changes in the ultra-structure occur by 589 µatm (i.e. in saturated waters). Finite element models of the algae grown at these heightened levels show an increase in the total strain energy of nearly an order of magnitude and an uneven distribution of the stress inside the skeleton when subjected to similar loads as algae grown at ambient levels. This weakening of the structure is likely to reduce the ability of the alga to resist boring by predators and wave energy with severe consequences to the benthic community structure in the immediate future (50 years).