Impacts of food availability and pCO2 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 (Omega) of seawater, is projected to have severe adverse consequences for calcifying organisms. While strong evidence suggests calcification by tropical reef-building corals containing algal symbionts (zooxanthellae) will decline over the next century, likely responses of azooxanthellate corals to ocean acidification are less well understood. Because azooxanthellate corals do not obtain photosynthetic energy from symbionts, they provide a system for studying the direct effects of acidification on energy available for calcification. The solitary azooxanthellate orange cup coral Balanophyllia elegans often lives in low-pH, upwelled waters along the California coast. In an 8-month factorial experiment, we measured the effects of three pCO2 treatments (410, 770, and 1220 µatm) and two feeding frequencies (3-day and 21-day intervals) on "planulation" (larval release) by adult B. elegans, and on the survival, skeletal growth, and calcification of newly settled juveniles. Planulation rates were affected by food level but not pCO2. Juvenile mortality was highest under high pCO2 (1220 µatm) and low food (21-day intervals). Feeding rate had a greater impact on calcification of B. elegans than pCO2. While net calcification was positive even at 1220 µatm (~3 times current atmospheric pCO2), overall calcification declined by ~25-45%, and skeletal density declined by ~35-45% as pCO2 increased from 410 to 1220 µatm. Aragonite crystal morphology changed at high pCO2, becoming significantly shorter but not wider at 1220 µatm. We conclude that food abundance is critical for azooxanthellate coral calcification, and that B. elegans may be partially protected from adverse consequences of ocean acidification in habitats with abundant heterotrophic food.

Food selectivity and processing by the cold-water coral Lophelia pertusa

Cold-water corals form prominent reef ecosystems along ocean margins that depend on suspended resources produced in surface waters. In this study, we investigated food processing of 13C and 15N labelled bacteria and algae by the cold-water coral Lophelia pertusa. Coral respiration, tissue incorporation of C and N and metabolic-derived C incorporation into the skeleton were traced following the additions of different food concentrations (100, 300, 1300 µg C/l) and two ratios of suspended bacterial and algal biomass (1:1, 3:1). Respiration and tissue incorporation by L. pertusa increased markedly following exposure to higher food concentrations. The net growth efficiency of L. pertusa was low (0.08±0.03), which is consistent with their slow growth rates. The contribution of algae and bacteria to total coral assimilation was proportional to the food mixture in the two lowest food concentrations, but algae were preferred over bacteria as food source at the highest food concentration. Similarly, the stoichiometric uptake of C and N was coupled in the low and medium food treatment, but was uncoupled in the high food treatment and indicated a comparatively higher uptake or retention of bacterial carbon as compared to algal nitrogen. We argue that behavioural responses for these small-sized food particles, such as tentacle behaviour, mucus trapping and physiological processing, are more likely to explain the observed food selectivity as compared to physical-mechanical considerations. A comparison of the experimental food conditions to natural organic carbon concentrations above CWC reefs suggests that L. pertusa is well adapted to exploit temporal pulses of high organic matter concentrations in the bottom water caused by internal waves and down-welling events.

Lipid, carbon and nitrogen content and fatty acid composition of Temora longicornis females and different food species during the experiment

Temora longicornis, a dominant calanoid copepod species in the North Sea, is characterised by low lipid reserves and high biomass turnover rates. To survive and reproduce successfully, this species needs continuous food supply and thus requires a highly flexible digestive system to exploit various food sources. Information on the capacity of digestive enzymes is scarce and therefore the aim of our study was to investigate the enzymatic capability to respond to quickly changing nutritional conditions. We conducted two feeding experiments with female T. longicornis from the southern North Sea off Helgoland. In the first experiment in 2005, we tested how digestive enzyme activities and enzyme patterns as revealed by substrate SDS-PAGE (sodium dodecylsulfate polyacrylamide gel electrophoresis) responded to changes in food composition. Females were incubated for three days fed ad libitum with either the heterotrophic dinoflagellate Oxyrrhis marina or the diatom Thalassiosira weissflogii. At the beginning and at the end of the experiment, copepods were deep-frozen for analyses. The lipolytic enzyme activity did not change over the course of the experiment but the enzyme patterns did, indicating a distinct diet-induced response. In a second experiment in 2008, we therefore focused on the enzyme patterns, testing how fast changes occur and whether feeding on the same algal species leads to similar patterns. In this experiment, we kept the females for 4 days at surplus food while changing the algal food species daily. At day 1, copepods were offered O. marina. On day 2, females received the cryptophycean Rhodomonas baltica followed by T. weissflogii on day 3. On day 4 copepods were again fed with O. marina. Each day, copepods were frozen for analysis by means of substrate SDS-PAGE. This showed that within 24 h new digestive enzymes appeared on the electrophoresis gels while others disappeared with the introduction of a new food species, and that the patterns were similar on day 1 and 4, when females were fed with O. marina. In addition, we monitored the fatty acid compositions of the copepods, and this indicated that specific algal fatty acids were quickly incorporated. With such short time lags between substrate availability and enzyme response, T. longicornis can successfully exploit short-term food sources and is thus well adapted to changes in food availability, as they often occur in its natural environment due seasonal variations in phyto- and microzooplankton distribution.

Habitat traits and food availability determine the response of marine invertebrates to ocean acidification

Energy availability and local adaptation are major components in mediating the effects of ocean acidification (OA) on marine species. In a long-term study, we investigated the effects of food availability and elevated pCO2 (ca 400, 1000 and 3000 µatm) on growth of newly settled Amphibalanus (Balanus) improvisus to reproduction, and on their offspring. We also compared two different populations, which were presumed to differ in their sensitivity to pCO2 due to differing habitat conditions: Kiel Fjord, Germany (Western Baltic Sea) with naturally strong pCO2 fluctuations, and the Tjärnö Archipelago, Sweden (Skagerrak) with far lower fluctuations. Over 20 weeks, survival, growth, reproduction and shell strength of Kiel barnacles were all unaffected by elevated pCO2, regardless of food availability. Moulting frequency and shell corrosion increased with increasing pCO2 in adults. Larval development and juvenile growth of the F1 generation were tolerant to increased pCO2, irrespective of parental treatment. In contrast, elevated pCO2 had a strong negative impact on survival of Tjärnö barnacles. Specimens from this population were able to withstand moderate levels of elevated pCO2 over 5 weeks when food was plentiful but showed reduced growth under food limitation. Severe levels of elevated pCO2 negatively impacted growth of Tjärnö barnacles in both food treatments. We demonstrate a conspicuously higher tolerance to elevated pCO2 in Kiel barnacles than in Tjärnö barnacles. This tolerance was carried-over from adults to their offspring. Our findings indicate that populations from fluctuating pCO2 environments are more tolerant to elevated pCO2 than populations from more stable pCO2 habitats. We furthermore provide evidence that energy availability can mediate the ability of barnacles to withstand moderate CO2 stress. Considering the high tolerance of Kiel specimens and the possibility to adapt over many generations, near future OA alone does not seem to present a major threat for A. improvisus