Effects of ocean acidification on learning in coral reef fishes

Ocean acidification has the potential to cause dramatic changes in marine ecosystems. Larval damselfish exposed to concentrations of CO2 predicted to occur in the mid- to late-century show maladaptive responses to predator cues. However, there is considerable variation both within and between species in CO2 effects, whereby some individuals are unaffected at particular CO2 concentrations while others show maladaptive responses to predator odour. Our goal was to test whether learning via chemical or visual information would be impaired by ocean acidification and ultimately, whether learning can mitigate the effects of ocean acidification by restoring the appropriate responses of prey to predators. Using two highly efficient and widespread mechanisms for predator learning, we compared the behaviour of pre-settlement damselfish Pomacentrus amboinensis that were exposed to 440 µatm CO2 (current day levels) or 850 µatm CO2, a concentration predicted to occur in the ocean before the end of this century. We found that, regardless of the method of learning, damselfish exposed to elevated CO2 failed to learn to respond appropriately to a common predator, the dottyback, Pseudochromis fuscus. To determine whether the lack of response was due to a failure in learning or rather a short-term shift in trade-offs preventing the fish from displaying overt antipredator responses, we conditioned 440 or 700 µatm-CO2 fish to learn to recognize a dottyback as a predator using injured conspecific cues, as in Experiment 1. When tested one day post-conditioning, CO2 exposed fish failed to respond to predator odour. When tested 5 days post-conditioning, CO2 exposed fish still failed to show an antipredator response to the dottyback odour, despite the fact that both control and CO2-treated fish responded to a general risk cue (injured conspecific cues). These results indicate that exposure to CO2 may alter the cognitive ability of juvenile fish and render learning ineffective.

The influence of ocean acidification on nitrogen regeneration and nitrous oxide production in the northwest European shelf sea

The assimilation and regeneration of dissolved inorganic nitrogen, and the concentration of N2O, was investigated at stations located in the NW European shelf sea during June/July 2011. These observational measurements within the photic zone demonstrated the simultaneous regeneration and assimilation of NH4+, NO2- and NO3-. NH4+ was assimilated at 1.82-49.12 nmol N/L/h and regenerated at 3.46-14.60 nmol N/L/h; NO2- was assimilated at 0-2.08 nmol N/L/h and regenerated at 0.01-1.85 nmol N/L/h; NO3-was assimilated at 0.67-18.75 nmol N/L/h and regenerated at 0.05-28.97 nmol N/L/h. Observations implied that these processes were closely coupled at the regional scale and that nitrogen recycling played an important role in sustaining phytoplankton growth during the summer. The [N2O], measured in water column profiles, was 10.13 ± 1.11 nmol/L and did not strongly diverge from atmospheric equilibrium indicating that sampled marine regions were neither a strong source nor sink of N2O to the atmosphere. Multivariate analysis of data describing water column biogeochemistry and its links to N-cycling activity failed to explain the observed variance in rates of N-regeneration and N-assimilation, possibly due to the limited number of process rate observations. In the surface waters of five further stations, ocean acidification (OA) bioassay experiments were conducted to investigate the response of NH4+ oxidising and regenerating organisms to simulated OA conditions, including the implications for [N2O]. Multivariate analysis was undertaken which considered the complete bioassay data set of measured variables describing changes in N-regeneration rate, [N2O] and the biogeochemical composition of seawater. While anticipating biogeochemical differences between locations, we aimed to test the hypothesis that the underlying mechanism through which pelagic N-regeneration responded to simulated OA conditions was independent of location. Our objective was to develop a mechanistic understanding of how NH4+ regeneration, NH4+ oxidation and N2O production responded to OA. Results indicated that N-regeneration process responses to OA treatments were location specific; no mechanistic understanding of how N-regeneration processes respond to OA in the surface ocean of the NW European shelf sea could be developed.

CO2 and vitamin B12 interactions determine bioactive trace metal requirements of a subarctic Pacific diatom

Phytoplankton growth can be limited by numerous inorganic nutrients and organic growth factors. Using the subarctic diatom Attheya sp. in culture studies, we examined how the availability of vitamin B(12) and carbon dioxide partial pressure (pCO(2)) influences growth rate, primary productivity, cellular iron (Fe), cobalt (Co), zinc (Zn) and cadmium (Cd) quotas, and the net use efficiencies (NUEs) of these bioactive trace metals (mol C fixed per mol cellular trace metal per day). Under B(12)-replete conditions, cells grown at high pCO(2) had lower Fe, Zn and Cd quotas, and used those trace metals more efficiently in comparison with cells grown at low pCO(2). At high pCO(2), B(12)-limited cells had ~50% lower specific growth and carbon fixation rates, and used Fe ~15-fold less efficiently, and Zn and Cd ~3-fold less efficiently, in comparison with B(12)-replete cells. The observed higher Fe, Zn and Cd NUE under high pCO(2)/B(12)-replete conditions are consistent with predicted downregulation of carbon-concentrating mechanisms. Co quotas of B(12)-replete cells were 5- to 14-fold higher in comparison with B(12)-limited cells, suggesting that >80% of cellular Co of B(12)-limited cells was likely from B(12). Our results demonstrate that CO(2) and vitamin B(12) interactively influence growth, carbon fixation, trace metal requirements and trace metal NUE of this diatom. This suggests the need to consider complex feedback interactions between multiple environmental factors for this biogeochemically critical group of phytoplankton in the last glacial maximum as well as the current and future changing ocean.

Short- and long-term conditioning of a temperate marine diatom community to acidification and warming

Ocean acidification and greenhouse warming will interactively influence competitive success of key phytoplankton groups such as diatoms, but how long-term responses to global change will affect community structure is unknown. We incubated a mixed natural diatom community from coastal New Zealand waters in a short-term (two-week) incubation experiment using a factorial matrix of warming and/or elevated pCO2 and measured effects on community structure. We then isolated the dominant diatoms in clonal cultures and conditioned them for 1 year under the same temperature and pCO2 conditions from which they were isolated, in order to allow for extended selection or acclimation by these abiotic environmental change factors in the absence of interspecific interactions. These conditioned isolates were then recombined into 'artificial' communities modelled after the original natural assemblage and allowed to compete under conditions identical to those in the short-term natural community experiment. In general, the resulting structure of both the unconditioned natural community and conditioned 'artificial' community experiments was similar, despite differences such as the loss of two species in the latter. pCO2 and temperature had both individual and interactive effects on community structure, but temperature was more influential, as warming significantly reduced species richness. In this case, our short-term manipulative experiment with a mixed natural assemblage spanning weeks served as a reasonable proxy to predict the effects of global change forcing on diatom community structure after the component species were conditioned in isolation over an extended timescale. Future studies will be required to assess whether or not this is also the case for other types of algal communities from other marine regimes.

In Situ effects of low pH and elevated HCO3 on juvenile massive Porites spp. in Moorea, French Polynesia

Juvenile colonies of massive Porites spp. were exposed to manipulated pH and bicarbonate ([HCO3-]) in situ to test the hypothesis that ocean acidification (OA) does not affect respiration and calcification. Incubations lasted 28 h and exposed corals to ambient temperature and light with ecologically relevant water motion. Three treatments were applied: (1) ambient conditions of pH 8.04 and 1751 µmol HCO3- kg(-1) (Treatment 1), (2) pCO2-induced ocean acidification of pH 7.73 and 2011 µmol HCO3- kg(-1) (Treatment 2), and (3) pCO2 and HCO3--enriched seawater of pH 7.69 and 2730 µmol HCO3- kg(-1) (Treatment 3). The third treatment providing elevated [HCO3-] was used to test for stimulatory effects of dissolved inorganic carbon on calcification under low pH and low saturation of aragonite (Omega arag), but it does not reflect conditions expected to occur under CO2-driven OA. Calcification of juvenile massive Porites spp. was affected by treatments, with an 81% elevation in Treatment 3 versus Treatment 1, but no difference between Treatments 1 and 2; respiration and the metabolic expenditure concurrent with calcification remained unaffected. These findings indicate that juvenile massive Porites spp. are resistant to short exposures to OA in situ, and separately, that they can increase calcification at low pH and low Omega arag if [HCO3-] is elevated. Juvenile Porites spp. may therefore be limited by dissolved inorganic carbon under ambient pCO2 conditions

Environmental controls on the Emiliania huxleyi calcite mass

Although ocean acidification is expected to impact (bio)calcification by decreasing the seawater carbonate ion concentration, [CO3]2-, there exists evidence of non-uniform response of marine calcifying plankton to low seawater [CO3]2-. This raises questions on the role of environmental factors other than acidification and on the complex physiological responses behind calcification. Here we investigate the synergistic effect of multiple environmental parameters, including temperature, nutrient (nitrate and phosphate) availability, and seawater carbonate chemistry on the coccolith calcite mass of the cosmopolitan coccolithophore Emiliania huxleyi, the most abundant species in the world ocean. We use a suite of surface (late Holocene) sediment samples from the South Atlantic and southwestern Indian Ocean taken from depths lying well above the modern lysocline. The coccolith calcite mass in our results presents a latitudinal distribution pattern that mimics the main oceanographic features, thereby pointing to the potential importance of phosphorus and temperature in determining coccolith mass by affecting primary calcification and possibly driving the E. huxleyi morphotype distribution. This evidence does not necessarily argue against the potentially important role of the rapidly changing seawater carbonate chemistry in the future, when unabated fossil fuel burning will likely perturb ocean chemistry beyond a critical point. Rather our study highlights the importance of evaluating the combined effect of several environmental stressors on calcifying organisms to project their physiological response(s) in a high CO2 world and improve interpretation of paleorecords.