Food availability and pCO2 impacts on planulation, juvenile survival, and calcification of the azooxanthellate scleractinian coral, Balanophyllia elegans

Ocean acidification, the assimilation of atmospheric CO₂ by the oceans that decreases the pH and CaCO₃ saturation state (Ω) of seawater, is projected to have severe consequences for calcifying organisms. Strong evidence suggests that tropical reef-building corals containing algal symbionts (zooxanthellae) will experience dramatic declines in calcification over the next century. The responses of azooxanthellate corals to ocean acidification are less well understood, and because they cannot obtain extra photosynthetic energy from symbionts, they provide a system for studying the direct effects of acidification on the energy available for calcification. The orange cup coral Balanophyllia elegans is a solitary, azooxanthellate scleractinian species common on the California coast where it thrives in the low pH waters of an upwelling regime. During an 8 month study, we addressed the effects of three pCO₂ treatments (410, 770, and 1230 μatm) and two feeding frequencies (High Food and Low Food) on adult Balanophyllia elegans planulation (larval release) rates, and on the survival, growth, and calcification of their juvenile offspring. Planulation rates were affected by food level but not pCO₂, while juvenile survival was highest under 410 μatm and High Food conditions. Our results suggest that feeding rate has a greater impact on calcification of B. elegans than pCO₂. Net calcification was positive even at 1230 μatm (~ 3 times current atmospheric pCO₂), although the increase from 410 to 1230 μatm reduced overall calcification by ~ 25–45%, and reduced skeletal density by ~ 35–45%. Higher pCO₂ also altered aragonite crystal morphology significantly. We discuss how feeding frequency affects azooxanthellate coral calcification, and how B. elegans may respond to ocean acidification in coastal upwelling waters.

The influence of food supply on the response of Olympia oyster larvae to ocean acidification

Increases in atmospheric carbon dioxide drive accompanying changes in the marine carbonate system as carbon dioxide (CO₂) enters seawater and alters its pH (termed “ocean acidification”). However, such changes do not occur in isolation, and other environmental factors have the potential to modulate the consequences of altered ocean chemistry. Given that physiological mechanisms used by organisms to confront acidification can be energetically costly, we explored the potential for food supply to influence the response of Olympia oyster (Ostrea lurida) larvae to ocean acidification. In laboratory experiments, we reared oyster larvae under a factorial combination of pCO₂ and food level. High food availability offset the negative consequences of elevated pCO₂ on larval shell growth and total dry weight. Low food availability, in contrast, exacerbated these impacts. In both cases, effects of food and pCO₂ interacted additively rather than synergistically, indicating that they operated independently. Despite the potential for abundant resources to counteract the consequences of ocean acidification, impacts were never completely negated, suggesting that even under conditions of enhanced primary production and elevated food availability, impacts of ocean acidification may still accrue in some consumers.

Calcification by juvenile corals under heterotrophy and elevated CO2

Ocean acidification (OA) threatens the existence of coral reefs by slowing the rate of calcium carbonate (CaCO₃) production of framework-building corals thus reducing the amount of CaCO₃ the reef can produce to counteract natural dissolution. Some evidence exists to suggest that elevated levels of dissolved inorganic nutrients can reduce the impact of OA on coral calcification. Here, we investigated the potential for enhanced energetic status of juvenile corals, achieved via heterotrophic feeding, to modulate the negative impact of OA on calcification. Larvae of the common Atlantic golf ball coral, Favia fragum, were collected and reared for 3 weeks under ambient (421 μatm) or significantly elevated (1,311 μatm) CO₂ conditions. The metamorphosed, zooxanthellate spat were either fed brine shrimp (i.e., received nutrition from photosynthesis plus heterotrophy) or not fed (i.e., primarily autotrophic). Regardless of CO₂ condition, the skeletons of fed corals exhibited accelerated development of septal cycles and were larger than those of unfed corals. At each CO₂ level, fed corals accreted more CaCO₃ than unfed corals, and fed corals reared under 1,311 μatm CO₂ accreted as much CaCO₃ as unfed corals reared under ambient CO₂. However, feeding did not alter the sensitivity of calcification to increased CO₂; ∆ calcification/∆Ω was comparable for fed and unfed corals. Our results suggest that calcification rates of nutritionally replete juvenile corals will decline as OA intensifies over the course of this century. Critically, however, such corals could maintain higher rates of skeletal growth and CaCO₃ production under OA than those in nutritionally limited environments.

Synergistic effects of pCO2 and iron availability on nutrient consumption ratio of the Bering Sea phytoplankton community

Little is known concerning the effect of CO₂ on phytoplankton ecophysiological processes under nutrient and trace element-limited conditions, because most of the CO₂ manipulation experiments have been conducted under these element-replete conditions. To investigate the effects of CO₂ and iron availability on phytoplankton ecophysiology, we conducted an experiment using a phytoplankton community in the iron-limited, high-nutrient, low-chlorophyll (HNLC) region of the Bering Sea basin in September 2009. Carbonate chemistry was controlled by the bubbling of the several levels of CO₂ concentration (180, 380, 600, and 1000 ppm) controlled air, and two iron conditions were established with or without the addition of inorganic iron. We demonstrated that in the iron-limited control conditions, the specific growth rate and the maximum photochemical quantum efficiency (F_v/F_m) of photosystem (PS) II decreased with increasing CO₂ levels, suggesting a~further decrease in iron bioavailability under the high CO₂ conditions. In addition, biogenic silica to particulate nitrogen and biogenic silica to particulate organic carbon ratios increased from 2.65 to 3.75 and 0.39 to 0.50, respectively with an increase in CO₂ level in the iron-limited controls. In contrast, in the iron-added treatments, specific growth rate, F_v/F_m values and elemental compositions did not change in response to the CO₂ variations, indicating that the addition of iron cancelled out the effect of the modulation of iron bioavailability due to the change in carbonate chemistry. Our results suggest that high CO₂ conditions can alter the biogeochemical cycling of nutrients through decreasing iron bioavailability in the iron-limited HNLC regions in the future.

Formation and maintenance of high-nitrate, low pH layers in the Eastern Indian Ocean and the role of nitrogen fixation

We investigate the biogeochemistry of Low Dissolved Oxygen High Nitrate layers forming against the backdrop of several interleaving regional water masses in the Eastern Indian Ocean, off northwest Australia adjacent to Ningaloo Reef. These water masses, including the forming Leeuwin Current, have been shown directly to impact the ecological function of Ningaloo Reef and other iconic coastal habitats downstream. Our results indicate that LODHN layers are formed from multiple subduction events of the Eastern Gyral Current beneath the Leeuwin Current (LC); the LC originates from both the Indonesian Throughflow and tropical Indian Ocean. Density differences of up to 0.025 kg m⁻³ between the Eastern Gyral Current and the Leeuwin Current produce sharp gradients that can trap high concentrations of particles (measured as low transmission) along the density interfaces. The oxidation of the trapped particulate matter results in local depletion of dissolved oxygen and regeneration of dissolved nitrate (nitrification). We document an associated increase in total dissolved carbon dioxide, which lowers the seawater pH by 0.04 units. Based on isotopic measurements (δ¹⁵N and δ¹⁸O) of dissolved nitrate, we determine that ∼40–100% of the nitrate found in LODHN layers is likely to originate from nitrogen fixation, and that regionally, the importance of N fixation in contributing to LODHN layers is likely be highest at the surface and offshore.

Effects of ocean acidification, temperature and nutrient regimes on the appendicularian Oikopleura dioica: a mesocosm study

Increasing pCO₂ is hypothesized to induce shifts in plankton communities toward smaller cells, reduced carbon export rates and increased roles of gelatinous zooplankton. Appendicularians, among the most numerous pan-global “gelatinous” zooplankton, continuously produce filter-feeding houses, shortcutting marine food webs by ingesting submicron particles, and their discarded houses contribute significantly to carbon fluxes. We present a first mesocosm-scale study on the effects of temperature, pCO₂ and bloom structures on the appendicularian, Oikopleura dioica. There were effects of temperature and nutrients on phytoplankton communities. No shifts in functional phytoplankton groups, nor changes in particle sizes/morphotypes, known to impact appendicularian feeding, were observed under manipulated pCO₂ conditions. However, appendicularian abundance was positively correlated with increased pCO₂, temperature and nutrient levels, consistent with hypotheses concerning gelatinous zooplankton in future oceans. This suggests appendicularians will play more important roles in marine pelagic communities and vertical carbon transport under projected ocean acidification and elevated temperature scenarios.

Effects of pCO2 and iron on the elemental composition and cell geometry of the marine diatom Pseudo-nitzschia pseudodelicatissima (Bacillariophyceae)

Partial pressure of CO₂ (pCO₂) and iron availability in seawater show corresponding changes due to biological and anthropogenic activities. The simultaneous change in these factors precludes an understanding of their independent effects on the ecophysiology of phytoplankton. In addition, there is a lack of data regarding the interactive effects of these factors on phytoplankton cellular stoichiometry, which is a key driving factor for the biogeochemical cycling of oceanic nutrients. Here, we investigated the effects of pCO₂ and iron availability on the elemental composition (C, N, P and Si) of the diatom Pseudo-nitzschia pseudodelicatissima (Hasle) Hasle by dilute batch cultures under 4 pCO₂ (~200, ~380, ~600, and ~800 μatm) and 5 dissolved inorganic iron (Fe′; ~5, ~10, ~20, ~50, and ~100 pmol. L⁻¹) conditions. Our experimental procedure successfully overcame the problems associated with simultaneous changes in pCO₂ and Fe′ by independently manipulating carbonate chemistry and iron speciation, which allowed us to evaluate the individual effects of pCO₂ and iron availability. We found that the C:N ratio decreased significantly only with an increase in Fe′, whereas the C:P ratio increased significantly only with an increase in pCO₂. Both Si:C and Si:N ratios decreased with increasing pCO₂ and Fe′. Our results indicate that changes in pCO₂ and iron availability could influence the biogeochemical cycling of nutrients in future oceans with high CO₂ levels, and, similarly, during the time course of phytoplankton blooms. Morever, pCO₂ and iron availability may also have affected oceanic nutrient biogeochemistry in the past, as these conditions have changed markedly over the Earth’s history.

Response of Nodularia spumigena to pCO2 – Part 2: Exudation and extracellular enzyme activities (update)

The filamentous and diazotrophic cyanobacterium Nodularia spumigena plays a major role in the productivity of the Baltic Sea as it forms extensive blooms regularly. Under phosphorus limiting conditions Nodularia spumigena have a high enzyme affinity for dissolved organic phosphorus (DOP) by production and release of alkaline phosphatase. Additionally, they are able to degrade proteinaceous compounds by expressing the extracellular enzyme leucine aminopeptidase. As atmospheric CO₂ concentrations are increasing, we expect marine phytoplankton to experience changes in several environmental parameters, including pH, temperature, and nutrient availability. The aim of this study was to investigate the combined effect of CO₂-induced changes in seawater carbonate chemistry and of phosphate deficiency on the exudation of organic matter, and its subsequent recycling by extracellular enzymes in a Nodularia spumigena culture. Batch cultures of Nodularia spumigena were grown for 15 days under aeration with low (180 μatm), medium (380 μatm), and high (780 μatm) CO₂ concentrations. Obtained pCO₂ levels in the treatments were on median 315, 353, and 548 μatm CO₂, respectively. Extracellular enzyme activities as well as changes in organic and inorganic compound concentrations were monitored. CO₂ treatment–related effects were identified for cyanobacterial growth, which in turn influenced the concentration of mucinous substances and the recycling of organic matter by extracellular enzymes. Biomass production was increased by 56.5% and 90.7% in the medium and high pCO₂ treatment, respectively, compared to the low pCO₂ treatment. In total, significantly more mucinous substances accumulated in the high pCO₂ treatment, reaching 363 μg Xeq L⁻¹ compared to 269 μg Xeq L⁻¹ in the low pCO₂ treatment. However, cell-specific rates did not change. After phosphate depletion, the acquisition of P from DOP by alkaline phosphatase was significantly enhanced. Alkaline phosphatase activities were increased by factor 1.64 and 2.25, respectively, in the medium and high compared to the low pCO₂ treatment. We hypothesise from our results that Nodularia spumigena can grow faster under elevated pCO₂ by enhancing the recycling of organic matter to acquire nutrients.

Effects of feeding and light intensity on the response of the coral Porites rus to ocean acidification

Recently, it has been suggested that there are conditions under which some coral species appear to be resistant to the effects of ocean acidification. To test if such resistance can be explained by environmental factors such as light and food availability, the present study investigated the effect of 3 feeding regimes crossed with 2 light levels on the response of the coral Porites rus to 2 levels of pCO₂ at 28 °C. After 1, 2, and 3 weeks of incubation under experimental conditions, none of the factors—including pCO₂—significantly affected area-normalized calcification and biomass-normalized calcification. Biomass also was unaffected during the first 2 weeks, but after 3 weeks, corals that were fed had more biomass per unit area than starved corals. These results suggest that P. rus is resistant to short-term exposure to high pCO₂, regardless of food availability and light intensity. P. rus might therefore represent a model system for exploring the genetic basis of tolerance to OA.

Modeling the dissolved CO2 system in the redox environment of the Baltic Sea

Generation and depletion of total alkalinity (A_T) were added to a Baltic Sea numerical model. The vertical distribution of generation and depletion of total alkalinity were described and attributed to different processes in the Eastern Gotland basin at the Gotland deep station (BY15) during the 1995–2004 period. At this site, the mean annual generation (28.2 µmol kg⁻¹ yr⁻¹) and depletion (−25.8 µmol kg⁻¹ yr⁻¹) were almost balanced, though the transient rates were much faster (+125/−340 µmol kg⁻¹ yr⁻¹). The mean volume-integrated A_T content increased up to 50 µmol kg⁻¹ when generation and depletion were added to the model. The A_T changes were coupled to oxidation–reduction (redox) reactions and the model budget indicates that internal generation and depletions is as important as lateral transports, including riverine input, at this site. Model predictive capability in marine environments with strong biogeochemical gradients was improved by coupling within the dissolved CO₂, and the biogeochemical, systems. This enables evaluation of eutrophication, acidification, and climate change simultaneously, and is important specifically in regions with permanent or periodic anoxia.