Net loss of CaCO 3 from coral reef communities due to human induced seawater acidification

Net loss of CaCO3 from coral reef communities due to human induced seawater acidification A. J. Andersson, I. B. Kuffner, F. T. Mackenzie, P. L. Jokiel, K. S. Rodgers, and A. Tan Bermuda Institute of Ocean Sciences, St. George’s, Bermuda US Geological Survey, Florida Integrated Science Center, St. Petersburg, FL, USA Department of Oceanography, University of Hawaii, Honolulu, HI, USA Hawaii Institute of Marine Biology, Kaneohe, HI, USA Received: 31 December 2008 – Accepted: 8 January 2009 – Published: Correspondence to: A. J. Andersson (andreas.andersson@bios.edu) Published by Copernicus Publications on behalf of the European Geosciences Union.


Introduction
A substantial fraction of the CO 2 released to the atmosphere from human activities is taken up by the ocean (e.g., Mackenzie et al., 2001;Sabine et al., 2004).CO 2 in solution produces carbonic acid (H 2 CO 3 ), which is a weak acid and results in a decrease in seawater pH (increasing acidity) and removal of carbonate ions (CO Introduction

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Full Screen / Esc Printer-friendly Version Interactive Discussion gration of these phases.Based on thermodynamic principles, precipitation of CaCO 3 is expected when Ω>1 and dissolution when Ω<1. Future model projections suggest that surface seawater pH will decrease 0.5-0.7 pH units relative to pre-industrial conditions in the next couple of centuries under a Business-As-Usual (BAU) CO 2 emission scenario (Caldeira and Wickett, 2003).Simultaneously, seawater saturation state with respect to carbonate minerals will decrease and seawater could become undersaturated in many environments with respect to high Mg-calcite minerals and even aragonite (Andersson et al., 2005;Orr et al., 2005).As a result, the ability to calcify and the rates of calcification among marine calcifiers are expected to decrease significantly.Additionally, the dissolution of carbonate sediments, structures, and even individual organisms could increase.These changes could be drastic and sufficiently large so that coral reef communities and carbonate ecosystems in general could become subject to a net loss of CaCO 3 material as a result of anthropogenic ocean acidification (Kleypas et al., 1999;Andersson et al., 2005Andersson et al., , 2007;;Yates and Halley, 2006;Hoegh-Guldberg et al., 2007).The effect of ocean acidification on carbonate dissolution has received relatively little attention compared to the effect of this process on organisms' ability to calcify despite the fact that it is more or less certain carbonate dissolution will increase in response to ocean acidification.
In the present study, we investigate the effects of future seawater conditions anticipated by the end of the present century and beyond on the community calcification (G) or what also has been referred to as the Net Ecosystem Calcification (NEC = CaCO 3 production -dissolution) (e.g., Andersson et al., 2005) of a typical subtropical coral reef community including its sediments incubated in mesocosms over a complete, 24-h, diel cycle.

Methods
The present diel investigation (21-22 June 2006) was a part of a longer term ocean acidification experiment conducted at the Hawaii Institute of Marine Biology (HIMB)  (Jokiel et al., 2008;Kuffner et al., 2008).Six 1×1×0.5-mfiberglass mesocosm tanks (Fig. 1) located in full sunlight were continuously supplied with flowing seawater pumped from approximately 2 m depth at the edge of the coral reef at a rate of approximately 7 to 8 l min −1 per mesocosm (turnover rate ∼1 h).Three mesocosms were randomly chosen to be maintained at an ambient chemical state with respect to seawater pCO 2 , pH, [CO 2− 3 ], and Ω.The remaining three mesocosms were maintained at a chemical state with respect to these parameters anticipated under a doubling of ambient seawater pCO 2 conditions.The carbonic-acid system was manipulated by constant addition of HCl (1.1 N) using a 205CA Watson Marlow multi-channel peristaltic pump at a rate of ∼1.3 ml min −1 .This produced a decrease in the seawater total alkalinity (TA) and a subsequent shift in the distribution of dissolved inorganic carbon species similar to that resulting from uptake of anthropogenic CO 2 (e.g., Langdon and Atkinson, 2005).Maintaining seawater flow and acid addition at constant rates ensured that natural fluctuations in seawater chemistry on both diel and seasonal cycles were preserved throughout the duration of the experiment (Kayanne et al., 1995;Ohde and van Woesik, 1999;Bates, 2002).Control mesocosms received plain tap water at the same rate acid was added to the treatment mesocosms.
Environmental and chemical parameters were measured in each mesocosm at least weekly in the long-term experiment to ensure that the desired treatment conditions were effective (Jokiel et al., 2008;Kuffner et al., 2008).During the diel experiment, in situ measurements were made and seawater samples collected every 2 and 4 h, respectively, in each mesocosm and also in the seawater intake lines for a duration of 24 h.Measured parameters included temperature and salinity (YSI 30 salinity/conductivity/temperature; ±0.1  (Lewis and Wallace, 1998) and stoichiometric dissociation constants defined by Mehrbach et al. (1973) and refit by Dickson and Millero (1987).Constants were redefined on the NBS scale.Although pH NBS measurements are not ideal for calculating the carbonic acid system in seawater, calculated ambient pCO 2 levels agreed well with independent measurements by a NOAA PMEL pCO 2 buoy located nearby to the seawater intake line (see supplemental information of Kuffner et al., 2008).Furthermore, it is the relative difference between treatment and control mesocosms that is most important in the present case.This difference is little affected by the shortcomings of the pH measurements.

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Full calcifiers were also present in each mesocosm as a result of natural settlement of larvae from the continuous flowing seawater (Jokiel et al., 2008;Kuffner et al., 2008).
Other non-calcifying organisms, including various algae, diatoms, cyanobacteria and sea hares, were also able to colonize the mesocosms in this manner.Nevertheless, forty colonies of M. capitata (Fig. 2) were by far the most important calcifying component of each mesocosm.Furthermore, a thin sediment layer of a few millimeters thickness comprised of very fine-grained carbonate material and organic debris was present at the bottom of each mesocosm.Some of this material came in through the seawater intake lines and settled out in the mesocosms, and some was produced in situ by the mechanical disintegration and as detritus from epiphytic borings of substrates of the biological community in the mesocosms.NEC was calculated according to the procedure outlined in Fig. 3 (see also supplementary Table S2, http://www.biogeosciences-discuss.net/6/1/2009/ bgd-6-1-2009-supplement.pdf).Statistical analysis of measured parameters was conducted using two-way analysis of variance (ANOVA) with mesocosms and time as fixed factors.Tukey's 1-degree of freedom test for non-additivity was used to evaluate interactions between the fixed factors.A priori contrasts of control and treatment mesocosms were used to evaluate the effects of treatment and formed the basis of the main statistical results reported here.

Results and discussion
Acidification of seawater in the treatment mesocosms resulted in a shift in the distribution of dissolved inorganic carbon parameters and produced conditions in the seawater with respect to pCO 2 , pH, CO 2− 3 and carbonate saturation state that could become reality by the end of this century and beyond as a result of continued anthropogenic emissions of CO 2 (Table 1; Fig. 4a, b).All these parameters were statistically significantly different between treatment and control mesocosms.Because of natural changes in seawater chemistry on diel time scales owing to metabolic pro-Introduction

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Full cesses (Kayanne et al., 1995;Ohde and van Woesik, 1999;Bates, 2002), neither control nor treatment chemical conditions were maintained at constant levels, but as anticipated varied significantly throughout a diel cycle.Both control and treatment mesocosms were subject to pCO 2 levels significantly higher than the current atmospheric pCO 2 and a doubling of the current level, respectively.However, it is important to realize that many coral reef environments are subject to surface seawater pCO 2 s much higher than the overlying atmosphere owing to processes such as calcification and remineraliztion of organic matter.For example, measurements in Kaneohe Bay made by E. DeCarlo and colleagues at the University of Hawaii and NOAA PMEL have on occassion shown surface seawater pCO 2 exceeding 1000 µatm at present time (http://www.pmel.noaa.gov/co2/coastal/kbay/CRIMP2all.htm).In the present study, the absolute difference between treatment and control mesocosms appeared greater at night than during the day, but the relative difference remained essentially constant throughout the 24-h period.On average, pCO 2 in the treatment mesocosms exceeded control mesocosms by 104±11%, pH was lower by 3.6±0.2%,and [CO 2− 3 ] and aragonite saturation state were both lower by 46±3%.Thus, the treatment effect represented a doubling of ambient conditions with respect to pCO 2 .The observed daytime and nighttime pCO 2 in treatment mesocosms roughly correspond to equilibrium levels with the atmosphere projected for year 2100 under emission scenarios B1 and A1FI, respectively (IPCC, 2001).The seawater saturation state with respect to aragonite was supersaturated in both control (Ω arag ∼3.6) and treatment (Ω arag ∼2.1) mesocosms during daytime.While control mesocosms remained supersaturated at night with respect to this mineral phase (Ω arag ∼2), treatment mesocosms reached values close to equilibrium (Ω arag =1.0).Consequently, the seawater was undersaturated with respect to carbonate minerals more soluble than aragonite, such as high Mg-calcite phases, at this time and potentially subject to dissolution.Daily average temperature, salinity and dissolved oxygen were close to identical in all mesocosms (Table 1).Nitrate and nitrite concentrations were statistically not different between treatment and control mesocosms, but concentrations of ammonium, phosphate and silicate were significantly different based on two-way ANOVA and a priori contrasts (Table 1).It is not clear whether the observed differences in these cases were due to the seawater acidification treatment or to other factors that were not accounted for.For example, average ammonium concentration was higher in the control relative to the treatment mesocosms.This was possibly due to nitrogen fixation by extensive mats of cyanobacteria observed on the mesocosm walls in two of the three control mesocosms.These mats reoccurred throughout the long-term experiment, and were observed in both control and treatment mesocosms with no obvious distinguishable pattern in their dynamics.Increases in ammonium concentration during incubations containing cyanobacteria have been observed and reported in other incubation studies (Kuffner and Paul, 2001).The reasons for the statistically significant differences in phosphate and silicate concentrations are unknown, but because the observed differences are small and the natural variability large (Table 1), there is little reason to suspect that these differences had any major direct or indirect effect on the observed TA and NEC.
The calculated NEC in control mesocosms consistently exceeded NEC in treatment mesocosms and the difference was statistically different (Table 1).Net calcification, i.e., net accumulation of CaCO 3 , was observed in both treatment and control mesocosms during daytime hours (Fig. 1).The highest daytime rate (±1std) of calcification was 9.7(6.2) mmol m −2 h −1 in the control mesocosms and 4.0(1.4)mmol m −2 h −1 in the treatment mesocosms.Net dissolution, i.e., net loss of CaCO 3 , was observed in both control and treatment mesocosms during nighttime.The highest dissolution rate (±1std) was −3.1(1.8)mmol m −2 h −1 in the control mesocosms and in the control mesocosms.In contrast, daily average dissolution exceeded calcification in the treatment mesocosms and gave rise to a loss of −0.1 mmol m −2 h −1 or −0.2 g CaCO 3 m −2 day −1 .These results are the net of living community metabolism as well as carbonate dissolution occurring in the thin sediment layer that accumulated at the bottom of the mesocosms.For a number of different studies investigating community calcification either in situ or in mesocosms for a range of different coral reef communities, substratum types, and CO 2 conditions, daily average net calcification rates range from −1 g CaCO 3 m −2 day −1 to 25 g CaCO 3 m −2 day −1 (e.g., Gattuso et al., 1996;Boucher et al., 1998;Langdon et al., 2000;Leclerq et al., 2002;Yates and Halley, 2006;Silverman et al., 2007).However, because of the large differences in experimental settings and conditions, it is not informative to make direct comparisons of results between these studies.Nevertheless, studies investigating the effect of rising levels of CO 2 and decreasing Ω showed a consistent decrease in the rate of community calcification concurrent with changes in these parameters (Langdon et al., 2000;Leclerq et al., 2002;Yates and Halley, 2006;Silverman et al., 2007).
The observed diel trend in NEC agrees with expectations based on theoretical and observational considerations.During daytime, primary production consumes CO 2 at a greater rate than respiration and microbial decomposition of organic matter produce CO 2 .This raises the seawater saturation state with respect to carbonate minerals and consequently favors more rapid calcification (e.g., Gattuso et al., 1999;Marubini et al., 2003;Langdon and Atkinson, 2005).Furthermore, photosynthesizing symbiotic algae provide their hosts, e.g., corals, with substantial amounts of energy that can be utilized for mechanisms such as the calcium-ATPase pump to control the chemistry of their internal calcifying fluid and thus enhance calcification (e.g., Cohen and McConnaughey, 2003).Corals calcify 3-5 times faster in light compared to dark conditions, which attests to the important coupling of this process to photosynthesis in these organisms (Gattuso et al., 1999).At nighttime, in the absence of photosynthesis, production of CO 2 from respiration lowers seawater saturation state with respect to carbonate minerals, which then could become subject to dissolution if the seawater becomes under-Introduction

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Interactive Discussion saturated with respect to a particular carbonate mineral phase.In the present case, the seawater of the treatment mesocosms was at times undersaturated with respect to all Mg-calcite minerals more soluble than aragonite; thus, these mineral phases potentially were subject to dissolution.In addition, chemical conditions in microenvironments were most likely even more corrosive to carbonate minerals owing to the metabolic activity of microbes, but also due to endolithic microorganisms known to colonize and actively penetrate carbonate substrates, i.e., bioerosion (e.g., Tribollet, 2008).Evidence of physical dissolution was observed in Mg-calcite producing rhodoliths that lost mass throughout the long-term experiment in the treatment mesocosms (Jokiel et al., 2008).Similarly, recruitment of crustose coralline algae depositing Mg-calcite containing 13-14 mol% MgCO 3 was significantly reduced by as much as 85% under treatment conditions (Jokiel et al., 2008;Kuffner et al., 2008).Physical and biological dissolution and disintegration processes probably produced much of the thin sediment layer that accumulated in the bottom of the tanks.This material is very fine-grained and thus has a high specific surface area making it very susceptible to dissolution.Despite the transition from net accumulation of CaCO 3 towards net dissolution under the current treatment conditions, the majority of individual coral colonies appeared healthy and gained mass throughout the long-term experiment, although at a slower rate relative to coral colonies in control mesocosms (Jokiel et al., 2008) shallow-water ocean environments worldwide (Milliman, 1993).Thus, the transition from net accumulation of CaCO 3 to a net loss represents a major reversal of a process that has been in effect for thousands of years.Interestingly, the transition to negative NEC acts as a weak negative feedback to rising anthropogenic CO 2 and ocean acidification since dissolution of calcium carbonate minerals consumes CO 2 through the reaction: Furthermore, this reaction increases alkalinity which further increases the capacity of the seawater to absorb more CO 2 .However, this process is slow relative to the rate at which human activities are changing the chemistry of surface seawater and it has been demonstrated that it will not produce sufficient alkalinity to produce a significant buffer effect on time scales of decades to centuries either on a global or a regional scale (e.g., Andersson et al., 2005).
Other investigators have attempted to define a critical threshold value with respect to either pCO 2 or [CO 2− 3 ] when dissolution will exceed calcification in different tropical and subtropical coral reef environments (Yates and Halley, 2006).However, such threshold values will vary significantly from environment to environment as a result of a myriad of factors that are difficult to account for accurately and depend on the temporal and spatial scale being considered.What is important in this context is the current trend and the relatively small changes in seawater chemistry required to reverse the net effect of marine calcification and carbonate dissolution.Some subtropical coral reef ecosystems, such as the coral reefs of Bermuda, may be subject to a net loss in CaCO 3 much sooner than ecosystems located at more tropical latitudes because of lower average seawater [CO 2− 3 ] and Ω (e.g., Kleypas et al., 1999).Intermediate, high latitude environments and associated cold water bioherms are even at greater risk since many of these environments currently exist at conditions close to equilibrium with aragonite (Orr et al., 2005;Guinotte et al., 2006).
Based on the current global socio-economic situation, it is highly unlikely that anthropogenic CO 2 emissions to the atmosphere will decrease significantly in the next

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Full Screen / Esc Printer-friendly Version Interactive Discussion several decades.Regardless of the effect of this additional CO 2 accumulating in the atmosphere on the magnitude of change of future global average temperature, which is still debated, the oceans will continue to absorb a significant fraction of this gas causing increasing acidity and all the potential ecological consequences associated with this major change in seawater chemistry.

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Silverman, J., Lazar, B., and Erez, J.: Effect of aragonite saturation, temperature, and nutrients on the community calcification rate of a coral reef, J. Geophys.Res., 112, C05004, doi:10.1029/2006JC003770,2007.Tribollet, A.: The boring microflora in modern coral reef ecosystems: a review of its roles, in: Current Developments in Bioerosion, edited by: Wisshak, M., and Tapanila, L., Springer-Verlag Berlin Heidelberg, 2008.Yates, K. K. and Halley, R. B.: CO 2− 3 concentration and pCO 2 thresholds for calcification and dissolution on the Molokai reef flat, Hawaii, Biogeosciences, 3, 357-369, 2006 the treatment mesocosms.Marginal positive calcification was observed during one measurement interval at night (0000-0400) in the control mesocosms, but the associated error suggests that these mesocosms could just as well have been subject to marginal dissolution during this time interval.Regardless, the two processes appeared closely balanced at this time.Daily average NEC and CaCO 3 accumulation were equal to 4.5 mmol CaCO 3 m −2 h −1 or 11 g CaCO 3 m − . The observed change in NEC between ambient and future seawater conditions is consistent with what we might expect as a result of lower seawater Ω, i.e., slower calcification and faster dissolution.However, the fact that the daily average NEC reached negative values under the prevailing chemical conditions of the treatment mesocosms has important implications for the oceanic inorganic carbon cycle, and the function and role of coral reefs and carbonate environments in the cycling of carbon should these conditions mimicking ocean acidification materialize in the natural environment.Since the seawater low stand of the last glacial maximum (∼18 000 years before present) and concurrent with the rise in sea level and the evolution of the present coastal ocean, significant accumulations of biologically produced CaCO 3 have occurred throughout calculated based on data from 12:00 to 08:00 *Rank transformation applied to data to meet assumptions of ANOVA

Figure 2 .
Figure 2. The calcifying community of each mesocosm was dominated by forty colonies of Montipora capitata.

Fig. 3 .
Fig. 3.The mesocosms are well mixed systems and can be represented by a simple box model.Assuming that changes in total alkalinity (TA) are uniquely attributed to calcification or carbonate dissolution, the Net Ecosystem Calcification (NEC) can be easily calculated according to equations I. to III. by measuring the TA of the inflowing (F inTA ) and outflowing (F outTA ) seawater, and the change in TA per unit time (d TA/dt) of the seawater in the mesocosms between consecutive sampling times.The NEC is multiplied by 2 owing to the fact that for every 1 mol of CaCO 3 precipitated or dissolved, 2 mol of TA is produced or removed.

Fig. 4 .
Fig. 4. (A) Seawater partial pressure of CO 2 (pCO 2 ) and (B), saturation state with respect to aragonite (Ω aragonite ) in the control (gray) and treatment (black) mesocosms as a function of time.The dashed line represents seawater equilibrium with respect to aragonite (Ω=1).(C) NEC in the control and treatment mesocosms during a complete diel cycle under the chemical conditions shown in (A) and (B).Positive values imply net calcification and negative values imply net dissolution.Error bars denote 1 standard deviation (n=3).

Table 1 .
. Introduction Average physical and chemical properties in control (n=3; white rows) and treatment mesocosms (n=3; gray rows) and results of statistical tests.Numbers in paranthesis represent 1 standard deviation.∆ is the average 24 h difference between control and treatment mesocosms relative to the former.

Table 1 .
Average physical and chemical properties in control (n=3; white rows) and treatment mesocosms (n=3; gray rows) and results of statistical tests.Numbers in paranthesis represent 1 standard deviation.∆ is the average 24 hour difference between control and treatment mesocosms relative to the former.