Calculating the global contribution of coralline algae to carbon burial

Introduction Conclusions References

Coralline algae are important contributors to the marine calcium carbonate (CaCO 3 ) deposited in the coral reef sediments (Goreau, 1963;Adey and Macintyre, 1973) and account for approximately 25 % of CaCO 3 accumulation within coastal regions (Martin et al., 2007). Calcifying photosynthesisers are both a sink and a source of CO 2 (Frankignoulle, 1994). Coralline algae act as a CO 2 sink in the processes of photosyn-10 thesis and CaCO 3 dissolution and act as a CO 2 source in the processes of respiration and CaCO 3 production (Martin et al., 2005(Martin et al., , 2006(Martin et al., , 2007(Martin et al., , 2013; Barron et al., 2006;Kamenos et al., 2013). We aim to estimate the global distribution of coralline algae, and from that, determine their potential role in long-term carbon burial. 15 The distribution and abundance of coralline algae is determined by ecological processes including growth, succession and competition (Steneck, 1986;McCoy and Kamenos, 2015) as well by environmental conditions such as disturbance, temperature and irradiance (Adey and Macintyre, 1973;Kamenos et al., 2004;Gattuso et al., 2006). Coralline algae grow both laterally to increase area and vertically to increase thick-20 ness (Steneck, 1986). Coralline algal vertical accretion rates vary widely from 0.1 to 80 mm yr −1 (Adey and McKibbin, 1970;Steneck and Adey, 1976;Edyvean and Ford, 1987). Succession in coralline algae is for thick and/or branched crusts to replace thinner unbranched crusts (Adey and Vassar, 1975;Steneck, 1986). Succession seems most rapid in the tropics, where colonization and succession takes ∼ 1 year, compared Introduction gae require disturbances, mainly herbivory as well as water motion, to remain clear of fleshy algae and invertebrates (Steneck, 1986). However, towed fishing gear (e.g. trawling) can easily damage rhodoliths (maerl) (Hall-Spencer and Moore, 2000;Kamenos and Moore, 2003). Overall, coralline algal distribution is likely primarily determined by irradiance and temperature (Adey and McKibbin, 1970;Adey and Adey, 1973;Gattuso 5 et al., 2006).

Surface covered by coralline algae
The surface of the coastal zone covered by coralline algae varies spatiotemporally and differs for free-living algae, geniculate and CCA (Supplement, cover ∼ 40 % of the reef slope (Littler and Doty, 1975;Stearn et al., 1977), 60 % of the reef flat and 5 % of lagoon sites (Atkinson and Grigg, 1984) with rhodoliths covering up 90 % of the reef crest (Sheveiko, 1981) and 90 % of the seaward shallow reef slope (Chisholm, 1988). Importantly, the area covered by coralline algae is not necessarily lower in regions dominated by other algal forms, because of their ability to occur on the 5 primary substratum (up to 90 %) or as epiphytes on larger algae (Johansen, 1981).

Processes and metabolism
While coralline algae are slow growing their high abundance and spatial distribution indicates their production is likely important (Johansen, 1981) and they are major contributors to the carbon-and carbonate cycles of coastal environments (Martin et al., 2013). 10 Organic production relates to the photosynthetic capacity of coralline algae, while inorganic production relates to the calcium carbonate production (Johansen, 1981).

Organic production
Organic production of coralline algae is low compared to other marine plants (Johansen, 1981;Steneck, 1986). However, because of their high abundance and world-15 wide dispersal, corallines can contribute significantly to the total marine primary production (Roberts et al., 2002). Production of 1 mole of organic material (photosynthesis) decreases dissolved inorganic carbon (DIC) by approximately 1 mole: Primary production also decreases pCO 2 , however the magnitude of these changes 20 depends on the equilibrium constants (Johansen, 1981). Respiration increases both DIC and pCO 2 (Johansen, 1981). Coralline algal respiration is between 20-60 % of gross primary production (Marsh, 1970;Littler, 1973;Littler and Murray, 1974;Sournia, 1976;Wanders, 1976). Net community production for coralline algae is induced 7850 Printer-friendly Version

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Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | or limited by environmental parameters including light reaching the communities (Gattuso et al., 2006;Martin et al., 2006;Burdett et al., 2014), temperature (Martin et al., 2006;Kamenos and Law, 2010) and nutrient availability (Smith et al., 2001). For example, Chisholm (2003) suggested that the high rates of productivity measured in situ at Lizard Island, Australia, came from the coralline algae that derive nutrients from the 5 underlying reef.

Inorganic production and accumulation
Photosynthesis also plays a crucial role in the production of inorganic material as it creates the environment in which calcification occurs (Johansen, 1981). The ratio of inorganic-organic production is high in coralline algae, compared to non-coralline sea-10 weeds (Johansen, 1981). Precipitation of CaCO 3 decreases DIC by 1 mole and total alkalinity by two equivalents for each mole precipitated: For calcium carbonate to be deposited an alkaline environment is required, as well as high concentrations of calcium and carbonate (Johansen, 1981). Calcification of 15 coralline algae occurs internally, compared to external calcification in corals and other invertebrates (Chisholm, 2003). The cell-walls of coralline algae are composed of calcium carbonate, and are mainly consist of high Mg-calcite (HMC: > 4 % wt of MgCO 3 ) (Moberly, 1968;Kamenos et al., 2008;Basso, 2012). The preservation of shallow-water carbonates is about 60 % and even up to 70-80 % if export is not taken into account 20 (Milliman, 1993).
Coralligenous algal-dominated rocky bottoms and rhodolith beds are among the highest algal carbonate producers when compared with Posidonia oceanica meadows, sandy bottom communities, Caulerpa-Cymodocea meadows, coralligenous animaldominated, photophilic algae and hemisciaphili algal communities (Canals and Ballesteros, 1997). The quantity of calcite production by coralline algae depends on their morphology (e.g., geniculate or non-geniculate, thick or thin crusts), growth rate and 7851 Introduction  (Littler, 1976) often over a season cycle (Martin et al., 2006). Martin et al. (2006) also observed a light limitation for the calcification of coralline algae.
Charpy-Roubaud and  suggest an area of 6.8 × 10 12 m 2 , because the average benthic photic zone of the world is smaller than 200 m. Here we will use 33 % 15 of the coastal zone which is the part of that receives enough light for photosynthesis (Gattuso et al., 2006) and thus assuming the production mainly occurs in the top 66 m of the coastal zone. Because coralline algae usually attach to harder substrata (Bosence, 1983) the surface covered by coralline algae (Supplement , Table S1) has to be taken into account. However, as there are substrates that have 0 % surface coverage 20 of coralline algae (e.g. on sandy substrata), to be conservative, we have assumed only half of the estimated surface coverage percentages estimated above contain coralline algae (CCA = 26.25 %, rhodoliths = 22.5 %, coralline algae = 22.5 %). At present we have an incomplete knowledge of the real distribution of coralline algae, so we estimate a global production based on the following parameters: the production of coralline Introduction

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Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | covered by coralline algae (22.5 %). We use the median in/organic C production for coralline algae due to skewed data distribution (Zar, 1999) across available studies.

Global coralline algal organic C production
Primary production by coralline algae ranges widely from 10 g C m −2 yr −1 by Lithothamnion coralloides in the Bay of Brest, France (Martin et al., 2006) to 2391 g C m −2 yr −1 5 by Hydrolithon onkodes at Lizard Island, Australia (Chisholm, 2003), giving a median production of 329 g C m −2 yr −1 (n = 39) ( Table 1) across depths and locations. Global C production may thus be as high as 0.7×10 9 t C yr −1 . The daily production of coralline algae corresponds with the range of production of benthic fleshy algae, turf algae, sand algae, phytoplankton, seagrasses and zooxanthellae (Table 2) and estimated yearly coralline algal production rate (329 g C m −2 yr −1 ) is in the range of production by mangroves, salt marshes and seagrasses and appears more productive than coastal phytoplankton, benthic diatoms and coral reefs (Table 2). Payri (2000) observed that the annual production of a coralline algal communities corresponds to approximately one third of the production of seagrass beds, which was also observed on the west-coast of 15 France with a production ratio of 3.12 (Martin et al., 2005). A production ratio of 1.5-3.7 is observed in this study when compared to seagrass production rate studies ( Table 2). The estimated production of free-living coralline algae (0.35 × 10 9 t C yr −1 ) is in the range determined by other studies while the production for CCA (0.88 × 10 9 t C yr −1 ) is slightly higher (Table 3). Thus, with a global oceanic production estimated at 20 48.5 × 10 9 t C yr −1 (Field et al., 1998) coralline algal production represent a measurable component.

Global inorganic coralline algal C production and accumulation
Studies focusing on coralline algae and calcium carbonate indicate a production range of 8-7400 g CaCO 3 m −2 yr −1 and a median of 880 g CaCO 3 m −2 yr −1 ( Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | was 1.8 × 10 9 t CaCO 3 yr −1 for coralline algae. Thus CaCO 3 production by coralline algae of 880 g CaCO 3 m −2 yr −1 lies within the range of coral reef calcite production of 75-4000 g CaCO 3 m −2 yr −1 (Canals and Ballesteros, 1997) and is comparable with the production rate in the Late Holocene ocean for coral reefs (1500 g CaCO 3 m −2 yr −1 (Milliman, 1993)). Basso (2012) estimated an average production rate of 5 g CaCO 3 m −2 yr −1 5 for the coralline algae in the Mediterranean sea, however this included coralline algae occurring below 100 m. Gattuso et al. (1998) suggested that communities in the coastal zone are responsible for more than 40 % (23×10 9 t CaCO 3 yr −1 ) of the total marine calcium carbonate production. Thus the estimated calcite production by coralline algae is similar to the production of other coastal communities (e.g. coral reefs, banks and 10 non/carbonate shelves) and might represent a large fraction of the coastal-and total ocean calcite production (Gattuso et al., 1998). Using average production rates for free-living algae and CCA an inorganic production was estimated for these two groups. The inorganic production for free-living algae was 22 g C-inorganic m −2 yr −1 and 147 g C-inorganic m −2 yr −1 for CCA. Thus inorganic 15 production by coralline algae of 105 g C-inorganic m −2 yr −1 and organic production of 330 g C-organic m −2 yr −1 gives a PIC : POC ratio of 0.32 (PIC is the particular inorganic carbon and POC the particular organic carbon). The PIC : POC ratio for free-living algae was 0.13 and 0.40 for the CCA. Significantly, a similar PIC : POC range of ratios of 0.23-0.29 was also observed for coccolithophores (Engel et al., 2005).

Global carbon accumulation
The long-term removal of C requires the fixed carbon to remain stored for 100-1000 years (Gattuso et al., 1998). The global long-term deposition rate of free-living coralline algae is 500 mm kyr −1 ( iment accretion of 70 mm kyr −1 , while for CCA this corresponds to a sediment accretion of 450 mm kyr −1 . Given the accretion rate of 500 mm kyr −1 , the preservation potential of coralline algae would be 64 %. This is consistent with the empirically calculated calcium carbonate preservation of 60 % (Milliman, 1993). However, if the preservation of CCA is excluded because of the lack of available accretion rates, and heavy grazing (Steneck, 5 1986), the preservation potential for this morphotype would be 14 %. As the complete preservation potential for coralline algae still required further refining, the potential carbon burial is estimated based on the sum of total organic production and the inorganic production. The estimated potential burial for the free-living algae was 0.4 × 10 9 and 1.2×10 9 t C yr −1 for CCA giving a potential carbon burial of 1.6×10 9 t C yr −1 for coralline 10 algae.

Future prospects: ocean acidification and rising temperature
Coralline algae may be vulnerable to the warming and lowering pH of sea water, caused by the currently occurring increase in anthropogenic CO 2 (Kleypas et al., 2006;McCoy and Kamenos, 2015). High pCO 2 conditions negatively affect the community growth The decreasing abundance and growth of coralline algae could have dramatic consequences for worldwide coastal ecosystems (Johansen, 1981;Martin and Gattuso, 2009;Basso, 2012). However, there is evidence that coralline algae will continue to calcify with increasing pCO 2 due to their high structural plasticity, but may be structurally and growth of algae due to increased pCO 2 availability (Hendriks et al., 2010). For example, Semesi et al. (2009) observed an increase in photosynthetic rates of coralline algae with a rising pCO 2 of seawater, however, whether this also translates to their accretion at longer time scales is still not clear.

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The ongoing increase of anthropogenic CO 2 is causing warming and acidification of world's ocean. Reduction of CO 2 to a sustainable level is required to avoid further environmental damage and various solutions have already been proposed. We calculate coralline algae to have a global average primary of 0.7 × 10 9 t C yr −1 and an estimated total global CaCO 3 production of 1.8 × 10 9 t CaCO 3 yr −1 which corresponds to an inor-10 ganic production of 0.2 × 10 9 t inorganic C yr −1 . With their substantial preservation potential and the longevity of the deposits they create, coralline algae have a significant capacity to store carbon. However, we are still uncertain of the impact future global change is likely to have on that capacity. Given their storage potential, empirical studies are now needed to refine the calculations.  Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K. B., Tignor, M., and Miller, H. L., Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, 749-832, 2007.  Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Stearn, C. W., Scoffin, T. P., and Martindale, W.: Calcium carbonate budget of a fringing reef on the west coast of Barbados, I: Zonation and productivity, Bull. Mar. Sci., 27, 479-510, 1977. Steneck, R. S.: The ecology of coralline algal crusts: convergent patterns and adaptative strategies, Annu. Rev. Ecol. Syst., 17, 273-303, 1986. Steneck, R. S. and Adey, W. H.: The role of environment in control of morphology in Lithophyl- 5 lum congestum, a Caribbean algal ridge builder, Bot. Mar., 19, 197-215, 1976 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Table 1. Primary production (daily and annual) of coralline algae (communities) from different depths and locations. Yearly primary production indicated in Italic are an estimate of the yearly production by taking a daily production and modifying this to a yearly production (x 365). The median production for crustose coralline algae and free-living algae is indicated. Charpy-Roubaud and