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Effects of Ocean Acidification on Calcification Of Biogeosciences, 8, 2089–2098, 2011 www.biogeosciences.net/8/2089/2011/ Biogeosciences doi:10.5194/bg-8-2089-2011 © Author(s) 2011. CC Attribution 3.0 License. Effects of ocean acidification on calcification of symbiont-bearing reef foraminifers K. Fujita1, M. Hikami1,2, A. Suzuki3, A. Kuroyanagi2, K. Sakai4, H. Kawahata2, and Y. Nojiri5 1Department of Physics and Earth Sciences, University of the Ryukyus, Okinawa, Japan 2Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Japan 3Geological Survey of Japan, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Japan 4Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus, Okinawa, Japan 5Center for Global Environmental Research, National Institute for Environmental Studies, Tsukuba, Japan Received: 2 February 2011 – Published in Biogeosciences Discuss.: 25 February 2011 Revised: 27 July 2011 – Accepted: 1 August 2011 – Published: 4 August 2011 Abstract. Ocean acidification (decreases in carbonate ion elevated pCO2, which induces CO2 fertilization effects by concentration and pH) in response to rising atmospheric algal symbionts, versus associated changes in seawater car- pCO2 is generally expected to reduce rates of calcification bonate chemistry, which decreases a carbonate concentra- by reef calcifying organisms, with potentially severe impli- tion. Our findings suggest that ongoing ocean acidification cations for coral reef ecosystems. Large, algal symbiont- might favor symbiont-bearing reef foraminifers with hya- bearing benthic foraminifers, which are important primary line shells at intermediate pCO2 levels (580 to 770 µatm) but and carbonate producers in coral reefs, produce high-Mg cal- be unfavorable to those with either hyaline or porcelaneous cite shells, whose solubility can exceed that of aragonite pro- shells at higher pCO2 levels (near 1000 µatm). duced by corals, making them the “first responder” in coral reefs to the decreasing carbonate saturation state of seawa- ter. Here we report results of culture experiments performed 1 Introduction to assess the effects of ongoing ocean acidification on the calcification of symbiont-bearing reef foraminifers using a The oceans have taken up about one-third of the anthro- high-precision pCO2 control system. Living clone individ- pogenic carbon dioxide released into the atmosphere over the uals of three foraminiferal species (Baculogypsina sphaeru- past 200 years (Sabine et al., 2004). According to the Inter- lata, Calcarina gaudichaudii, and Amphisorus hemprichii) governmental Panel on Climate Change (IPCC) Special Re- were subjected to seawater at five pCO2 levels from 260 to port on Emission Scenarios (SRES), atmospheric CO2 will 970 µatm. Cultured individuals were maintained for about 12 rise further, up to a partial pressure of 500–1000 µatm by the weeks in an indoor flow-through system under constant wa- end of the century (Meehl et al., 2007). This absorption of ter temperature, light intensity, and photoperiod. After the CO2 into the surface ocean changes seawater chemistry, re- experiments, the shell diameter and weight of each cultured sulting in decreases in pH and carbonate ion concentration, specimen were measured. Net calcification of B. sphaeru- and increases in the concentrations of bicarbonate and hy- lata and C. gaudichaudii, which secrete a hyaline shell and drogen ions. It will also lead to a decrease in the saturation host diatom symbionts, increased under intermediate levels state of seawater with respect to calcite and aragonite, two of pCO2 (580 and/or 770 µatm) and decreased at a higher common forms of calcium carbonate secreted by marine cal- pCO2 level (970 µatm). Net calcification of A. hemprichii, cifying organisms (Orr et al., 2005). Calcification of marine which secretes a porcelaneous shell and hosts dinoflagel- calcareous organisms is strongly dependent on the carbonate late symbionts, tended to decrease at elevated pCO2. Ob- saturation state of seawater, suggesting that ocean acidifica- served different responses between hyaline and porcelaneous tion will adversely affect marine calcifying taxa, with po- species are possibly caused by the relative importance of tentially severe implications for marine ecosystems such as coral reefs (Kleypas et al., 1999). Correspondence to: K. Fujita ([email protected]) Published by Copernicus Publications on behalf of the European Geosciences Union. 2090 K. Fujita et al.: Effects of ocean acidification on calcification Culture experiments with reef calcifying organisms such 2 Materials and methods as corals, coralline algae, molluscs, and foraminifers suggest that ocean acidification will adversely impact their calcifica- 2.1 Target species tion (e.g. Gattuso et al., 1998; Kuffner et al., 2008; Kuroy- anagi et al., 2009; Ries et al., 2009), leading to a reduction in Three species of large, algal symbiont-bearing benthic coral-reef biodiversity and the net accumulation of reef car- foraminifers were selected for this study: Baculogypsina bonates in the future (Hoegh-Guldberg et al., 2007). Large, sphaerulata (Parker and Jones), Calcarina gaudichaudii reef-dwelling benthic foraminifers (defined as mature indi- d’Orbigny in Ehrenberg, and Amphisorus hemprichii Ehren- viduals > 1 mm in diameter) are shelled protists that are host berg. These species are commonly found on macrophytes to algal endosymbionts (Lee, 1998; Hallock, 1999). They on coral-reef flats in the northwest Pacific (e.g. Hoheneg- are one of the primary producers and carbonate producers in ger, 1994) and are important primary producers and carbon- coral reefs (Hallock, 1981; Langer et al., 1997; Hohenegger, ate producers in their environments (e.g. Sakai and Nishihira, 2006; Fujita and Fujimura, 2008), secreting high-magnesium 1981; Hohenegger, 2006; Fujita and Fujimura, 2008). Shells calcite (HMC; Raja et al., 2005), the solubility of which of all three species are composed of high-magnesium calcite can exceed that of aragonite at a similar seawater pCO 2 (HMC; approx. 10 Mg mol %; Saraswati et al., 2004). Shell level (Morse et al., 2006). Therefore, reef foraminifers with walls of B. sphaerulata and C. gaudichaudii are perforate high-magnesium calcite shells may be the “first responders” and have a hyaline (i.e. clear, glassy) appearance, whereas among reef calcifying organisms to the decreasing saturation those of A. hemprichii are imperforate and appear porcela- state of seawater caused by ocean acidification. neous (i.e. shiny, white, and smooth like porcelain). Baculo- During calcification, foraminifers are able to elevate the gypsina sphaerulata and C. gaudichaudii are host to diatom pH at the site of calcification (vesicles or seawater vac- endosymbionts, whereas A. hemprichii is host to dinoflag- uoles) by one unit above seawater pH (Erez, 2003; Ben- ellate endosymbionts (Lee, 1998). In addition, these three tov et al., 2009; de Nooijer et al., 2009). In acidified species have been observed to reproduce asexually during seawater, foraminifers would require more energy to ele- spring and summer (Sakai and Nishihira, 1981; Hoheneg- vate the intracellular pH, leading to a decrease in calcifi- ger, 2006). Thus, asexually reproduced clone individuals can cation. Previous culturing results have indicated that shell be used for culture experiments to exclude the effect of ge- weights of both planktonic and benthic foraminifers reduce netic variability on the experimental results. For more de- with decreasing [CO2−] or pH (Bijma et al., 1999, 2002; 3 tailed information on the taxonomy, biology, and ecology of Dissard et al., 2010; Lombard et al., 2010). Calcification these species, see Rottger¨ and Kruger¨ (1990) and Hoheneg- (measured as increments of shell weight and diameter) of ger (1994). Marginopora, a large, dinoflagellate symbiont-bearing ben- thic foraminifer, is reduced as pH becomes lower (Kuroy- anagi et al., 2009). Culture experiments using 14C tracer 2.2 Maintenance until asexual reproduction techniques of reef foraminifers have also shown that the car- bon uptake ratio is dependent on pH and concentrations of Adult individuals just before asexual reproduction (agamont inorganic carbon and calcium, and decreases when the pH or or shizont) were collected during low tide on nearshore the concentrations of these elements are lower than those of reef flats: B. sphaerulata and C. gaudichaudii northeast of the present seawater (ter Kuile et al., 1989). Ikei Island, Okinawa, Japan (26◦230 N, 128◦000E) on 26 However, the effects of ocean acidification on calcification April and 22 May 2009, and A. hemprichii on a reef moat of diverse large, algal symbiont-bearing and reef-dwelling along the Oudo coast, south of Okinawa Island (26◦050 N, benthic foraminifers have been assessed in only one species 127◦420 E) on 28 May 2009. Collected individuals were (Marginopora kudakajimensis; Kuroyanagi et al., 2009). Re- maintained separately in small Petri dishes filled with natu- cent studies have shown that the response of marine calcify- ral seawater at room temperature (approximately 25 ◦C) un- ing organisms to ocean acidification varies both within and der a natural light:dark cycle near a window (light inten- among species (e.g. Fabry, 2008; Langer et al., 2009; Ries sity, ∼100 µmol m−2 s−1). Because C. gaudichaudii and et al., 2009; Ridgwell et al., 2009). Moreover, in our previ- B. sphaerulata are commonly found in high-energy reef-flat ous study (Kuroyanagi et al., 2009), we controlled the pH environments (Hohenegger, 1994), these species
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