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Perspective on the Response of Marine Calcifiers to Global Warming And Kawahata et al. Progress in Earth and Planetary Science (2019) 6:5 Progress in Earth and https://doi.org/10.1186/s40645-018-0239-9 Planetary Science REVIEW Open Access Perspective on the response of marine calcifiers to global warming and ocean acidification—Behavior of corals and foraminifera in a high CO2 world “hot house” Hodaka Kawahata1,2*, Kazuhiko Fujita3, Akira Iguchi2, Mayuri Inoue4, Shinya Iwasaki5, Azumi Kuroyanagi6, Ayumi Maeda1, Takuya Manaka7, Kazuyoshi Moriya8, Haruka Takagi1, Takashi Toyofuku5, Toshihiro Yoshimura5 and Atsushi Suzuki2 Abstract The CO2 concentration of air has increased over the last two centuries and recently surpassed 400 ppm. Carbon cycle models project CO2 concentrations of 720 to 1000 ppm for the IPCC intermediate scenario (RCP 6.0), resulting in an increase in global mean temperature of ~ 2.6 °C and a decrease in seawater pH of ~ 0.3. Together, global warming and ocean acidification are often referred to as the “evil twins” of climate change, potentially inducing severe threats in the near future. In this paper, our discussion is focused on the response of two major calcifiers, foraminifera and corals, which contribute much to the global carbonate burial rate. Photosymbiosis is regarded as an adaptive ecology for living in warm and oligotrophic oceans, especially for reef-building corals and larger reef- dwelling benthic foraminifera. As a consequence of global warming, bleaching may be a global threat to algal symbiont-bearing marine calcifying organisms under conditions of high temperature and light intensity. If CO2 is dissolved in seawater, the partial pressure of CO2 in seawater (pCO2) and dissolved inorganic carbon (DIC) increases while pH and the saturation state of carbonate minerals decreases without any change in total alkalinity. Generally, marine calcifying organisms show decreases in calcification rates in response to acidified seawater. However, the response often differs depending on situations, species, and life-cycle stage. Some benthic foraminifera showed a positive response to low pH conditions. The Acropora digitifera coral calcification of adult branches was not reduced markedly at higher pCO2 conditions, although calcification tended to decrease versus pCO2 in both aposymbiotic and symbiotic polyps. New analytical technologies help identify important constraints on calcification processes. Based upon Ca isotopes, the transport path of Ca2+ and the degree of its activity would predominantly control the carbonate precipitation rate. Visualization of the extracellular pH distribution shows that proton pumping produces the high internal pH and large internal–external pH gap in association with foraminiferal calcification. From the perspective of a long-term change in the Earth’s surface environment, foraminifera seem to be more adaptive and robust than corals in coping with ocean warming and acidification but it is necessary to further understand the mechanisms underlying variations in sensitivity to heat stress and acidified seawater for future prediction. Since CO2 is more soluble in lower temperature seawater, ocean acidification is more critical in the polar and high-latitude (Continued on next page) * Correspondence: [email protected] 1Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan 2Geological Survey of Japan, National Institute of Advanced Industrial Science and Technology (AIST), Higashi 1-1-1, Tsukuba, Ibaraki 305-8567, Japan Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. Kawahata et al. Progress in Earth and Planetary Science (2019) 6:5 Page 2 of 37 (Continued from previous page) regions. Additionally, older deep-water has enhanced acidity owing to the addition of CO2 from the degradation of organic matter via a synergistic effect with high pressure. With current ocean acidification, pH and the saturation state of carbonate minerals are decreasing without any change in total alkalinity. However, in the Earth’s history, it is well known that alkalinity has fluctuated significantly. Therefore, it is necessary to quantitatively reconstruct alkalinity, which is another key factor determining the saturation state of carbonate minerals. The rapid release of anthropogenic CO2 (in the present day and at the Paleocene/Eocene boundary) induces severe ocean acidification, whereas in the Cretaceous, slow environmental change, even at high levels of pCO2, could raise alkalinity, thereby neutralizing ocean acidification. Keywords: Partial pressure of CO2, Global warming, Ocean acidification, Coral, Foraminifera, Bleaching, Calcite, Aragonite, Saturation state, Organic matter, Alkalinity, Carbon cycle Introduction El Nino/Southern Oscillation phenomena (e.g., Beaufort Human beings are now dramatically changing our planet and Grelaud 2017). and altering the environment by modifying the global car- In oligotrophic environments such as coral reefs and sub- bon cycle through anthropogenic carbon dioxide (CO2) tropical gyres in the Pacific, the symbiotic relationship be- emissions from the burning of fossil fuels. The CO2 concen- tween the host and its symbiotic algae presents three major tration of air was around 280 ppm in 1750 AD (the begin- advantages: energy from photosynthesis, an enhancement ning of Industrial Revolution), but it has increased over the of calcification, and uptake of host metabolites. Bleaching is last two centuries and is currently above 400 ppm. Carbon defined as (i) damage to the symbiotic relationships be- dioxideisoneoftheprimarygreenhousegasesinEarth’sat- tween hosts and algal symbionts and (ii) photosynthetic mosphere, together with water vapor, methane, nitrous pigment loss (Iglesias-Prieto et al. 1992). Elevated seawater oxide, and others. The Intergovernmental Panel on Climate temperature brings negative effects on marine calcifiers; in Change (IPCC) intermediate RCP 6.0 scenarios (IPCC particular, coral bleaching has occurred repeatedly since 2013b) predicts that the CO2 concentration in air will in- 1979 AD (e.g., Bunkley-Williams and Williams 1990)in crease to 720–1000 ppm by 2100 AD and that the global tropical regions worldwide (Brown 1997;Hoegh- mean temperature will rise by 2.6 °C. Comparison of CO2 Guldberg et al. 2007). Mass bleaching events such as those concentrations in the atmosphere with fossil-fuel burning in 1979–1980 AD, 1982–1983 AD, and 1986–1988 AD data indicates that about 60% of fossil-fuel emissions remain provide important opportunities for investigating the in- intheair.Theremainderismainlyabsorbedbytheocean, fluence of bleaching during the early stages of this re- which may provide some relief from severe warming. search area. Recently, bleaching has been found in benthic Atmospheric carbon reservoirs are controlled by the for- foraminifera in coral reefs (Schmidt et al. 2011). Coral mation/dissolution of both carbonate and organic matter reefs are among the ecosystems most vulnerable to envir- (OM) in the ocean, which changes the chemical equilib- onmental stresses associated with future climate changes rium of the marine CO2 system by removing/adding alka- caused by human activities (IPCC 2017). linity in association with the release/absorbance of CO2 in By the end of twenty-first century, the surface waters of the atmosphere (Fig. 1) (e.g., Kleypas et al. 1999; Kleypas the ocean could be more acidic, resulting in an undersatur- et al. 2006; Orr et al. 2005). In open ocean, biogenic car- ation condition with respect to carbonate minerals in some bonate production is positively correlated with biogenic areas of high latitude. Ocean acidification (OA) will induce OM production, although the carbon ratios of OM to car- severe stress in calcifiers, some of which are sensitive to en- bonate generally increase as OM fluxes increase (based vironmental changes at global and local levels. Additionally, upon the results from sediment trap experiments in the Oschlies et al. (2008) pointed out that anthropogenic CO2 Pacific Kawahata 2002). Planktic foraminifera, which live emissions will extend oxygen-minimum zones, a 50% in- −3 in the ocean surface layers from tropical to polar regions, crease in the suboxic (defined as dissolved O2 < 5 mmol m ) secrete low-Mg calcite shells and contribute 32–80% of water volume by the end of this century, although a serious the total deep-marine calcite budget in the global carbon- ocean anoxic event, which occurred in the Cretaceous, will ate cycle (Schiebel 2002). The comparable carbonate con- not occur in the normal open ocean. Drivers such as OA, tributor in the open ocean is coccolithophore. This is a higher seawater temperature, or reduced dissolved oxygen unicellular, eukaryotic phytoplankton (alga) and one of the concentration may overlap to amplify ecosystem impacts. more abundant primary producers in the ocean, espe- Therefore, understanding the effect of environmental cially in tropical and subtropical oceans influenced by parameters (i.e., temperature, salinity, pH, and dissolved Kawahata et al. Progress in Earth and Planetary Science (2019) 6:5 Page 3 of 37
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