Growth response of an early successional assemblage of coralline algae and benthic diatoms to ocean acidification

The sustained absorption of anthropogenically released atmospheric CO2 by the oceans is modifying seawater carbonate chemistry, a process termed ocean acidification (OA). By the year 2100, the worst case scenario is a decline in the average oceanic surface seawater pH by 0.3 units to 7.75. The changing seawater carbonate chemistry is predicted to negatively affect many marine species, particularly calcifying organisms such as coralline algae, while species such as diatoms and fleshy seaweed are predicted to be little affected or may even benefit from OA. It has been hypothesized in previous work that the direct negative effects imposed on coralline algae, and the direct positive effects on fleshy seaweeds and diatoms under a future high CO2 ocean could result in a reduced ability of corallines to compete with diatoms and fleshy seaweed for space in the future. In a 6-week laboratory experiment, we examined the effect of pH 7.60 (pH predicted to occur due to ocean acidification just beyond the year 2100) compared to pH 8.05 (present day) on the lateral growth rates of an early successional, cold-temperate species assemblage dominated by crustose coralline algae and benthic diatoms. Crustose coralline algae and benthic diatoms maintained positive growth rates in both pH treatments. The growth rates of coralline algae were three times lower at pH 7.60, and a non-significant decline in diatom growth meant that proportions of the two functional groups remained similar over the course of the experiment. Our results do not support our hypothesis that benthic diatoms will outcompete crustose coralline algae under future pH conditions. However, while crustose coralline algae were able to maintain their presence in this benthic rocky reef species assemblage, the reduced growth rates suggest that they will be less capable of recolonizing after disturbance events, which could result in reduced coralline cover under OA conditions.

Effects of ocean acidification on population dynamics and community structure of crustose coralline algae

Calcification and growth of crustose coralline algae (CCA) are affected by elevated seawater pCO2 and associated changes in carbonate chemistry. However, the effects of ocean acidification (OA) on population and community-level responses of CCA have barely been investigated. We explored changes in community structure and population dynamics (size structure and reproduction) of CCA in response to OA. Recruited from an experimental flow-through system, CCA settled onto the walls of plastic aquaria and developed under exposure to one of three pCO2 treatments (control [present day, 389±6 ppm CO2], medium [753±11 ppm], and high [1267±19 ppm]). Elevated pCO2 reduced total CCA abundance and affected community structure, in particular the density of the dominant species Pneophyllum sp. and Porolithon onkodes. Meanwhile, the relative abundance of P. onkodes declined from 24% under control CO2 to 8.3% in high CO2 (65% change), while the relative abundance of Pneophyllum sp. remained constant. Population size structure of P. onkodes differed significantly across treatments, with fewer larger individuals under high CO2. In contrast, the population size structure and number of reproductive structures (conceptacles) per crust of Pneophyllum sp. was similar across treatments. The difference in the magnitude of the response of species abundance and population size structure between species may have the potential to induce species composition changes in the future. These results demonstrate that the impacts of OA on key coral reef builders go beyond declines in calcification and growth, and suggest important changes to aspects of population dynamics and community ecology.

Skeletal trade-offs in coralline algae in response to ocean acidification

Ocean acidification is changing the marine environment, with potentially serious consequences for many organisms. Much of our understanding of ocean acidification effects comes from laboratory experiments, which demonstrate physiological responses over relatively short timescales. Observational studies and, more recently, experimental studies in natural systems suggest that ocean acidification will alter the structure of seaweed communities. Here, we provide a mechanistic understanding of altered competitive dynamics among a group of seaweeds, the crustose coralline algae (CCA). We compare CCA from historical experiments (1981-1997) with specimens from recent, identical experiments (2012) to describe morphological changes over this time period, which coincides with acidification of seawater in the Northeastern Pacific. Traditionally thick species decreased in thickness by a factor of 2.0-2.3, but did not experience a change in internal skeletal metrics. In contrast, traditionally thin species remained approximately the same thickness but reduced their total carbonate tissue by making thinner inter-filament cell walls. These changes represent alternative mechanisms for the reduction of calcium carbonate production in CCA and suggest energetic trade-offs related to the cost of building and maintaining a calcium carbonate skeleton as pH declines. Our classification of stress response by morphological type may be generalizable to CCA at other sites, as well as to other calcifying organisms with species-specific differences in morphological types.

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.

Nongeniculate coralline algae from IODP Site 310-M0005D

Material cored during the Integrated Ocean Drilling Program (IODP) Expedition 310 'Tahiti Sea Level' revealed that the fossil reef systems around Tahiti are composed of two major stratigraphic sequences: (i) a last deglacial sequence; and (ii) an older Pleistocene sequence. The older Pleistocene carbonate sequence is composed of reef deposits associated with volcaniclastic sediments and was preserved in Hole 310-M0005D drilled off Maraa. Within an approximately 70-m-thick older Pleistocene sequence (33.22-101.93 m below seafloor; 92.85-161.56 m below present sealevel) in this hole, 11 depositional units are defined by lithological changes, sedimentological features, and paleontological characteristics and are numbered sequentially from the top of the hole downward (Subunits P1-P11). Paleowater depths inferred from nongeniculate coralline algae, combined with those determined by using corals and larger foraminifers, suggest two major sealevel rises during the deposition of the older Pleistocene sequence. Of these, the second sealevel rise is associated with an intervening sealevel drop. It is likely that the second sealevel rise corresponds to that during Termination II (TII, the penultimate deglaciation, from Marine Isotope Stages 6 to 5e). Therefore, the intervening sealevel drop can be correlated with that known as the 'sealevel reversal' during TII. Because there are limited data on the Pleistocene reef systems in the tropical South Pacific Ocean, this study provides important information about Pleistocene sealevel history, the evolution of coral reef ecosystems, and the responses of coral reefs to Quaternary climate changes.

Adenylate concentration and energy charge in different thallus regions and after UV radiation in brown, red and green algae

A method was developed to extract adenine nucleotides AMP, ADP, and ATP from marine macroalgal tissue to gain information on the cellular energy charge. Quantification was carried out by high performance liquid chromatography (HPLC). Three species from the rocky shore of the island of Helgoland (German Bight) were examined: Laminaria saccharina (Phaeophyta), Chondrus crispus (Rhodophyta), and Ulva lactuca (Chlorophyta). In L. saccharina and C. crispus, the adenylate energy charge (AEC) was determined in different thallus regions. AEC varied in relation to tissue age and function. Higher AEC values typically occurred in thallus regions with meristematic activity. Furthermore, L. saccharina and U. lactuca were exposed to UV-A and elevated UV-B radiation. The AEC was calculated and the maximal quantum yield of photosystem II (Fv/Fm) was determined as indicators for UV stress. In both species, the AEC remained at high values (0.72 ± 0.04), while Fv/Fm dropped rapidly. The results show that the photosynthesis of the phaeophyte is more resistant to UV radiation than the chlorophyte.

Seawater carbonate chemistry and settlement of a spawning coral on three common species of crustose coralline algae

Concern about the impacts of ocean acidification (OA) on ecosystem function has prompted many studies to focus on larval recruitment, demonstrating declines in settlement and early growth at elevated CO2 concentrations. Since larval settlement is often driven by particular cues governed by crustose coralline algae (CCA), it is important to determine whether OA reduces larval recruitment with specific CCA and the generality of any effects. We tested the effect of elevated CO2 on the survival and settlement of larvae from the common spawning coral Acropora selago with 3 ecologically important species of CCA, Porolithon onkodes, Sporolithon sp., and Titanoderma sp. After 3 d in no-choice laboratory assays at 447, 705, and 1214 µatm pCO2, the rates of coral settlement declined as pCO2 increased with all CCA taxa. The magnitude of the effect was highest with Titanoderma sp., decreasing by 87% from the ambient to highest CO2 treatment. In general, there were high rates of larval mortality, which were greater with the P. onkodes and Sporolithon sp. treatments (~80%) compared to the Titanoderma sp. treatment (65%). There was an increase in larval mortality as pCO2 increased, but this was variable among the CCA species. It appears that OA reduces coral settlement by rapidly altering the chemical cues associated with the CCA thalli and microbial community, and potentially by directly affecting larval viability.

Seawater carbonate chemistry and structural integrity of the coralline algae Lithothamnion glaciale in a laboratory experiment

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).

Diffusion boundary layers ameliorate the negative effects of ocean acidification on the temperate coralline macroalga Arthrocardia corymbosa

Anthropogenically-modulated reductions in pH, termed ocean acidification, could pose a major threat to the physiological performance, stocks, and biodiversity of calcifiers and may devalue their ecosystem services. Recent debate has focussed on the need to develop approaches to arrest the potential negative impacts of ocean acidification on ecosystems dominated by calcareous organisms. In this study, we demonstrate the role of a discrete (i.e. diffusion) boundary layer (DBL), formed at the surface of some calcifying species under slow flows, in buffering them from the corrosive effects of low pH seawater. The coralline macroalga Arthrocardia corymbosa was grown in a multifactorial experiment with two mean pH levels (8.05 'ambient' and 7.65 a worst case 'ocean acidification' scenario projected for 2100), each with two levels of seawater flow (fast and slow, i.e. DBL thin or thick). Coralline algae grown under slow flows with thick DBLs (i.e., unstirred with regular replenishment of seawater to their surface) maintained net growth and calcification at pH 7.65 whereas those in higher flows with thin DBLs had net dissolution. Growth under ambient seawater pH (8.05) was not significantly different in thin and thick DBL treatments. No other measured diagnostic (recruit sizes and numbers, photosynthetic metrics, %C, %N, %MgCO3) responded to the effects of reduced seawater pH. Thus, flow conditions that promote the formation of thick DBLs, may enhance the subsistence of calcifiers by creating localised hydrodynamic conditions where metabolic activity ameliorates the negative impacts of ocean acidification.

Ocean acidification alleviates low-temperature effects on growth and photosynthesis of the red alga Neosiphonia harveyi (Rhodophyta)

This study aimed to examine interactive effects between ocean acidification and temperature on the photosynthetic and growth performance of Neosiphonia harveyi. N. harveyi was cultivated at 10 and 17.5 °C at present (~380 µatm), expected future (~800 µatm), and high (~1500 µatm) pCO2. Chlorophyll a fluorescence, net photosynthesis, and growth were measured. The state of the carbon-concentrating mechanism (CCM) was examined by pH-drift experiments (with algae cultivated at 10 °C only) using ethoxyzolamide, an inhibitor of external and internal carbonic anhydrases (exCA and intCA, respectively). Furthermore, the inhibitory effect of acetazolamide (an inhibitor of exCA) and Tris (an inhibitor of the acidification of the diffusive boundary layer) on net photosynthesis was measured at both temperatures. Temperature affected photosynthesis (in terms of photosynthetic efficiency, light saturation point, and net photosynthesis) and growth at present pCO2, but these effects decreased with increasing pCO2. The relevance of the CCM decreased at 10 °C. A pCO2 effect on the CCM could only be shown if intCA and exCA were inhibited. The experiments demonstrate for the first time interactions between ocean acidification and temperature on the performance of a non-calcifying macroalga and show that the effects of low temperature on photosynthesis can be alleviated by increasing pCO2. The findings indicate that the carbon acquisition mediated by exCA and acidification of the diffusive boundary layer decrease at low temperatures but are not affected by the cultivation level of pCO2, whereas the activity of intCA is affected by pCO2. Ecologically, the findings suggest that ocean acidification might affect the biogeographical distribution of N. harveyi.

Effect of ocean acidification and pH fluctuations on the growth and development of coralline algal recruits, and an associated benthic algal assemblage

Coralline algae are susceptible to the changes in the seawater carbonate system associated with ocean acidification (OA). However, the coastal environments in which corallines grow are subject to large daily pH fluctuations which may affect their responses to OA. Here, we followed the growth and development of the juvenile coralline alga Arthrocardia corymbosa, which had recruited into experimental conditions during a prior experiment, using a novel OA laboratory culture system to simulate the pH fluctuations observed within a kelp forest. Microscopic life history stages are considered more susceptible to environmental stress than adult stages; we compared the responses of newly recruited A. corymbosa to static and fluctuating seawater pH with those of their field-collected parents. Recruits were cultivated for 16 weeks under static pH 8.05 and 7.65, representing ambient and 4*preindustrial pCO2 concentrations, respectively, and two fluctuating pH treatments of daily (daytime pH = 8.45, night-time pH = 7.65) and daily (daytime pH = 8.05, night-time pH = 7.25). Positive growth rates of new recruits were recorded in all treatments, and were highest under static pH 8.05 and lowest under fluctuating pH 7.65. This pattern was similar to the adults' response, except that adults had zero growth under fluctuating pH 7.65. The % dry weight of MgCO3 in calcite of the juveniles was reduced from 10% at pH 8.05 to 8% at pH 7.65, but there was no effect of pH fluctuation. A wide range of fleshy macroalgae and at least 6 species of benthic diatoms recruited across all experimental treatments, from cryptic spores associated with the adult A. corymbosa. There was no effect of experimental treatment on the growth of the benthic diatoms. On the community level, pH-sensitive species may survive lower pH in the presence of diatoms and fleshy macroalgae, whose high metabolic activity may raise the pH of the local microhabitat.

Seawater carbonate chemistry and calcification of the crustose coralline alga Hydrolithon onkodes in a laboratory experiment

Anthropogenic CO2 emissions have exacerbated two environmental stressors, global climate warming and ocean acidification (OA), that have serious implications for marine ecosystems. Coral reefs are vulnerable to climate change yet few studies have explored the potential for interactive effects of warming temperature and OA on an important coral reef calcifier, crustose coralline algae (CCA). Coralline algae serve many important ecosystem functions on coral reefs and are one of the most sensitive organisms to ocean acidification. We investigated the effects of elevated pCO2 and temperature on calcification of Hydrolithon onkodes, an important species of reef-building coralline algae, and the subsequent effects on susceptibility to grazing by sea urchins. H. onkodes was exposed to a fully factorial combination of pCO2 (420, 530, 830 µatm) and temperature (26, 29 °C) treatments, and calcification was measured by the change in buoyant weight after 21 days of treatment exposure. Temperature and pCO2 had a significant interactive effect on net calcification of H. onkodes that was driven by the increased calcification response to moderately elevated pCO2. We demonstrate that the CCA calcification response was variable and non-linear, and that there was a trend for highest calcification at ambient temperature. H. onkodes then was exposed to grazing by the sea urchin Echinothrix diadema, and grazing was quantified by the change in CCA buoyant weight from grazing trials. E. diadema removed 60% more CaCO3 from H. onkodes grown at high temperature and high pCO2 than at ambient temperature and low pCO2. The increased susceptibility to grazing in the high pCO2 treatment is among the first evidence indicating the potential for cascading effects of OA and temperature on coral reef organisms and their ecological interactions.