Reviews and syntheses: Calculating the global contribution of coralline algae to total carbon burial

The ongoing increase in anthropogenic carbon dioxide (CO2) emissions is changing the global marine environment and is causing warming and acidification of the oceans. Reduction of CO2 to a sustainable level is required to avoid further marine change. Many studies investigate the potential of marine carbon sinks (e.g. seagrass) to mitigate anthropogenic emissions, however, information on storage by coralline algae and the beds they create is scant. Calcifying photosynthetic organisms, including coralline algae, can act as a CO2 sink via photosynthesis and CaCO3 dissolution and act as a CO2 source during respiration and CaCO3 production on short-term timescales. Longterm carbon storage potential might come from the accumulation of coralline algae deposits over geological timescales. Here, the carbon storage potential of coralline algae is assessed using meta-analysis of their global organic and inorganic carbon production and the processes involved in this metabolism. Net organic and inorganic production were estimated at 330 g C m yr and 900 g CaCO3 m −2 yr respectively giving global organic/inorganic C production of 0.7/1.8× 10 t C yr. Calcium carbonate production by free-living/crustose coralline algae (CCA) corresponded to a sediment accretion of 70/450 mm kyr. Using this potential carbon storage for coralline algae, the global production of free-living algae/CCA was 0.4/1.2× 10 t C yr suggesting a total potential carbon sink of 1.6× 10 tonnes per year. Coralline algae therefore have production rates similar to mangroves, salt marshes and seagrasses representing an as yet unquantified but significant carbon store, however, further empirical investigations are needed to determine the dynamics and stability of that store. 1 Carbon storage and coralline algae An increase in exploitation of fossil fuels since the mid-18th century caused a rise in the partial pressure of carbon dioxide in both atmospheric (CO2) and oceanic (pCO2) reservoirs (Sabine et al., 2004; Meehl et al., 2007). Atmospheric CO2 has risen from 280 ppm in 1750 (Denman et al., 2007) to nearly 400 ppm in 2014 (Diugokencky and Tans, 2015) at a rate unprecedented in geological history (Denman et al., 2007). The marine environment has been changing rapidly in the last few centuries too (Cubasch et al., 2013), with increasing CO2 causing warming and acidification of the Earth’s oceans (Caldeira and Wickett, 2005). Concentrations of atmospheric CO2 simulated by coupled climate-carbon cycle models range between 730 and 1200 ppm by 2100 (Meehl et al., 2007). Therefore, a reduction of atmospheric CO2 to a sustainable level is needed to avoid further environmental damage (Collins et al., 2013; Kirtman et al., 2013). The oceans are a major sink of anthropogenic CO2 emissions, accounting for ∼ 48 % of emissions absorption since the Industrial Revolution (Sabine et al., 2004). Significantly, around 50 % of the global primary production (which uses pCO2) is by marine organisms (Beardall and Raven, 2004) with marine microalgae and bacteria being the dominant source of primary production and respiration (Duarte and Cebrian, 1996; del Giorgio and Duarte, 2002; Duarte et al., 2005). Vegetated marine habitats, including macroalgae and seagrasses, are often neglected from accounts of the global ocean carbon cycle because of their limited extent (cover < 2 % of ocean surface; Duarte and Cebrian, 1996). However, vegetated coastal habitats have a great carbon storage Published by Copernicus Publications on behalf of the European Geosciences Union. 6430 L. H. van der Heijden and N. A. Kamenos: Calculating the global contribution of coralline algae capacity (Duarte et al., 2005) and the potential of marine coastal vegetation as a sink for anthropogenic carbon emissions (blue carbon) is becoming of interest (Nellemann et al., 2009). These marine macrophyte ecosystems have slow turnover rates and are therefore more effective carbon sinks than planktonic ecosystems (Smith, 1981). Red coralline algae are present from the tropics to polar regions (Johansen, 1981; Steneck, 1986; Foster, 2001; Wilson, 2004). Coralline algae are important for ecosystems due to their role in carbon cycling, creating and maintaining habitats, and reef building/structuring roles (Nelson, 2009). They are divided in two morpho-functional groups; geniculated (articulated) and non-geniculated (non-articulated; Johansen, 1981). The morphological states range from totally adherent to having non-adherent margins (leafy) to totally non-adherent (free-living, e.g. rhodoliths, maerls and nodules; Steneck, 1986; Cabioch, 1988). The calcium carbonate skeleton of coralline algae prevents them from breaking down quickly compared to fleshy algae (Borowitzka, 1982; Wilson, 2004). Coralline algal species have been observed in the fossil record since the early Cretaceous (Aguirre et al., 2000) and coralline algal communities reach 500–800 years (Adey and Macintyre, 1973; Kamenos, 2010) with ∼ 8000year-old free-living coralline algal beds present in France (Birkett et al., 1998). Coralline algae are important contributors to the marine calcium carbonate (CaCO3) deposited in the coral reef sediments (Goreau, 1963; Adey and Macintyre, 1973) and account for approximately 25 % of CaCO3 accumulation within coastal regions (Martin et al., 2007). Calcifying photosynthesisers are both a sink and a source of CO2 (Frankignoulle, 1994). Coralline algae act as a CO2 sink in the processes of photosynthesis and CaCO3 dissolution and act as a CO2 source in the processes of respiration and CaCO3 production (Martin et al., 2005, 2006, 2007, 2013a; 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 total carbon burial. 2 Coralline algal succession and small-scale distribution 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 as 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 thickness (Steneck, 1986). Coralline algal vertical accretion rates vary widely from 0.1 to 80 mm yr (Adey and McKibbin, 1970; Steneck and Adey, 1976; Edyvean and Ford, 1987). Succession in coralline algae occurs when thick and/or branched crusts 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 to 6–7 years in the boreal North Pacific and > 10 years in the subarctic North Atlantic (Steneck, 1986; McCoy and Ragazzola, 2014). In shallow productive zones coralline algae 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 et al., 2006). 2.1 Global distribution Coralline algae are ecosystem engineers (Nelson, 2009), major framework builders and carbonate producers, especially in temperate and cold water benthic ecosystems (Nelson, 1988; Freiwald and Henrich, 1994; Foster, 2001; Gherardi, 2004; Bracchi and Basso, 2012; Savini et al., 2012; Basso, 2012). Coralline algae are found from the low intertidal to the infralittoral and circalittoral zones (> 200 m depth; Steneck, 1986; Basso, 1998; Foster, 2001) and have a worldwide spatial distribution (Fig. 1; Table S2 in the Supplement). While crustose coralline algae (CCA) grow exclusively on hard surfaces, free-living coralline algae are able to form rhodoliths when they settle on non-cohesive particulate substrates or are detached from existing hard substrates by fragmentation (Bosence, 1983). 2.2 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 (Table S1). The average coralline algal sea bed coverage from published studies is 52.5 % for CCA, 45.0 % for rhodoliths and 45.0 % for coralline algae overall. Figueiredo et al. (2008) indicate that the surface covered by CCA on the Abrolhos Bank (20 900 km) in Brazil ranges from 5–40 % on the reef flats, 30–80 % on the reef crests and 10–50 % on the reef walls with coverage varying due to differences in the abundance of turf algae and herbivory pressure. On coral reefs, CCA (e.g. Porolithon onkodes) can 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 primary substratum (up to 90 %) or as epiphytes on larger algae (Johansen, 1981). Biogeosciences, 12, 6429–6441, 2015 www.biogeosciences.net/12/6429/2015/ L. H. van der Heijden and N. A. Kamenos: Calculating the global contribution of coralline algae 6431 Figure 1. The global distribution of the three coralline algae Families (Corallinaceae, Hapalidiaceae and Sporolithaceae; for species list per country/region see Table S2). The numbers indicate: 1. Spitsbergen, 2. Iceland, 3. Greenland, east, 4. Greenland, 5. Canada, Arctic, 6. Canada, Labrador, 7. Canada, Newfoundland, 8. Canada, New Brunswick, 9. Canada, Nova Scotia, 10. USA, Aleutian Islands, Alaska, 11. USA, Alaska, 12. Revillagigedo Islands, USA, 13. Canada, British Columbia, 14. Canada, Queen Charlotte Islands, 15. USA, Washington, 16. USA, Oregon, 17. USA, California, 18. USA, Channel Islands, California, 19. Mexico, Baja California, 20. Mexico, Isla Guadalupe, 21. USA, Gulf of California, 22. USA, Maine, 23. USA, New Hampshire, 24. USA, Connecticut, 25. USA, Virginia, 26. USA, North Carolina, 27. USA, South Carolina, 28. USA, Florida, 29. USA, Texas, 30. Mexico, 31. Belize, 32. Honduras, 33. El Salvador, 34. Nicaragua, 35. Costa Rica, 36. Panama, 37. Cuba, 38. Bahamas, 39. Caicos Islands, 40. Jamaica, 41. Hispaniola, Dominican Republic, 42. Puerto Rico, 43. Virgin Islands, USA, 44. Saints Kitts, 45. Martinique, 46. Barbados, 47. Saint Thomas, Barbados, 48. Lesser Antilles, 49. Trinidad, 50. Tobago, 51. Trinidad and Tobago, 52. Curacao, 53. Netherlands Antilles, 54. Tropical and Subtropical Western Atlantic, 55. Guyana, 56. Aves, island of Venezuela, 57. Venezuela, 58. Colombia, 59. Ecuador, 60. Galapagos Islands, 61. Peru, 62. Chile, 63. Brazil, 64. Uruguay, 65. Argentina, 66. Falkland Islands, 67. Gough Island, 68. Saint Helena, 69. Ascension, 70. Cape Verde Islands, 71. Canary Islands, 72. Portugal, Salvage Islands, 73. Madeira, 74. Azores, 75. Bermuda, 76. Norway, 77. Sweden, 78. Scandinavia, 79. Baltic Sea, 80. Faroe Islands, 81. Great-Britain, 82. Ireland, 83. Netherlands, 84. France, 85. Spain, 86. Portugal, 87. Gibraltar, 88. Spain, Isla de Alboran, 89. Balearic Islands, Spain, 90. Monaco, 91. Corsica, 92. Sardinia, 93. Italy, 94. Sicily, 95. Malta, 96. Italy, Pelagie Islands, 97. Italy, Adriatic Sea, 98. Slovenia, 99. Croatia, 100. Albania, 101. Greece, 102. Bulgaria, 103. Romania, 104. Black Sea, 105. Turkey, 106. Cyprus, 107. Syria, 108. Israel, 109. Saudi Arabia, 110. Red Sea, 111. Yemen, 112. Oman, 113. Dubai, 114. Abu Dhabi, 115. Qatar, 116. Bahrain, 117. Kuwait, 118. Iran, 119. Persian Gulf, 120. Djibouti, 121. Eritrea, 122. Sudan, 123. Egypt, Red Sea, 124. Egypt, 125. Libya, 126. Tunisia, 127. Algeria, 128. Morocco, 129. Western Sahara, 130. Mauritania, 131. Senegal, 132. Gambia, 133. Sierra Leone, 134. Liberia, 135. Cote d’Ivoire, 136. Ghana, 137. Nigeria, 138. Cameroon, 139. Equatorial Guinea, 140. São Tomé and Principe, 141. Gabon, 142. Congo, 143. Angola, 144. Namibia, 145. South Africa, 146. Mozambique, 147. Madagascar, 148. Tanzania, 149. Kenya, 150. Somalia, 151. Ethiopia, 152. Pakistan, 153. India, 154. Sri Lanka, 155. Bangladesh, 156. Comores and Mayotte, 157. Aldabra Islands, 158. Réunion, 159. Mauritius, 160. Seychelles, 161. Amirante Islands, 162. Saya de Malha Bank, 163. Cargados Carajos, 164. Rodrigues Island, 165. India, Laccadive Islands, 166. Maldives, 167. Chagos Archipelago, 168. Diego Garcia Atoll, 169. Amsterdam Island, 170. Cocos (Keeling) Islands, 171. Andaman Islands, India, 172. Nicobar Islands, India, 173. Indian Ocean Islands, 174. Myanmar, 175. Thailand, 176. Malaysia, 177. Vietnam, 178. Singapore, 179. Philippines, 180. Indonesia, 181. Indonesia, New Guinea, 182. Taiwan, 183. China, 184. Hong Kong, 185. Japan, 186. Korea, 187. Russia, east, 188. Russia, Kamchatka, 189. Russia, Commander Islands, 190. Saint Paul Island, 191. Easter Island, 192. Northwestern Hawaiian Islands, USA, 193. Hawaiian Islands, USA, 194. Wake Atoll, 195. Ryukyu Islands, Japan, 196. Mariana Islands, 197. Guam, 198. Republic of Palau, 199. Federated States of Micronesia, 200. Marshall Islands, 201. Tuvalu, 202. Samoan Archipelago, 203. American Samoa, 204. Central Polynesia, 205. French Polynesia, 206. Tahiti, 207. Fiji, 208. Solomon Islands, 209. Papua New Guinea, 210. Christmas Island, Australia, 211. Australia, western , 212. Australia, Houtman Abrolhos, 213. Australia, Northern Territory, 214. Australia, Queensland, 215. Australia, New South Wales, 216. Australia, Lord Howe Island, 217. Australia, Norfolk Island, 218. Australia, Victoria, 219. Australia, Bass Strait, 220. Australia, South, 221. Tasmania, 222. New Zealand, 223. New Zealand, Stewart Islands/Rakiura, 224. New Zealand, Snares Islands/Tini Heke, 225. New Zealand, Auckland Islands, 226. New Zealand, Kermadec Islands, 227. New Zealand, Chatman Islands, 228. New Zealand, Bounty Island, 229. New Zealand, Antipodes Islands, 230. Antarctica, Campbell Islands, 231. Antarctica, Macquarie Island, 232. Antarctica, Heard Island, 233. Antarctica, Kerguelen, 234. Antarctica, Crozet Islands, 235. Antarctica, South Georgia, 236. Antarctica, South Orkney Islands, 237. Antarctica, South Shetland Islands, 238. Antarctica, Fuegia, 239. Antarctica, Tierra del Fuego, 240. Antarctica, Peninsula, and 241. Antarctica, Subantarctic Islands. www.biogeosciences.net/12/6429/2015/ Biogeosciences, 12, 6429–6441, 2015 6432 L. H. van der Heijden and N. A. Kamenos: Calculating the global contribution of coralline algae Table 1. Net primary production (daily and annual) of coralline algae (communities) from different depths and locations. Yearly primary production indicated in italics are an estimate of the yearly production by taking a daily production and modifying this to a yearly production (× 365). The median production for crustose coralline algae and free-living algae is indicated. Structure or species Location Depth Primary production Primary production Reference (g C m−2 d−1) (g C m−2 yr−1) Crustose coralline algae 370 This study (n= 35) Crustose coralline algae San Salvador Island, Bahamas 81 m 0.07 26 Littler et al. (1986) Hydrolithon spp. Klein Piscadera, Curacao 25 m 0.21 77 Vooren (1981) Sporolithon ptychoides Klein Piscadera, Curacao 25 m 0.21 78 Vooren (1981) Pseudolithoderma nigrum Wilson Cove, California, USA 0.40 146 Littler and Murray (1974) Sporolithon erythraeum Waikiki reef, Hawaii, USA 0.50 183 Littler (1973) Porolithon onkodes Waikiki reef, Hawaii, USA 0.50 183 Littler (1973) Porolithon gardineri Waikiki reef, Hawaii, USA 0.50 183 Littler (1973) Hydrolithon decipiens Wilson Cove, California, USA 0.50 183 Littler and Murray (1974) Phymatolithon foecundum + P. Tenue Young Sound, NE Greenland 17–36 m 70–300 Roberts et al. (2002) Reef building coralline algae Eniwetok Atoll, Hawaii, USA 2 m 0.66 240 Marsh (1970) Porolithon conicum Lizard Island, Australia 0–18 m 0.18–1.16 66–423 Chisholm (1988) Lithophyllum sp. Coral reef, Curacao 0.5–3 m 0.70 256 Wanders (1976) Neogoniolithon fosliei Lizard Island, Australia 0–6 m 0.46–0.95 168–347 Chisholm (1988) Porolithon onkodes Lizard Island, Australia 0–6 m 0.37–1.35 135–493 Chisholm (1988) Hydrolithon reinboldii Lizard Island, Australia 3–6 m 0.86–0.90 314–329 Chisholm (1988) Lithophyllum intermedium Coral reef, Curacao 0.5–3 m 0.90 329 Wanders (1976) Lithophyllum congestum Coral reef, Curacao 0.5–3 m 1.00 365 Wanders (1976) Crustose coralline algae Coral reef, Curacao 0.5–3 m 1.00 370 Wanders (1976) Porolithon pachydermum Coral reef, Curacao 0.5–3 m 1.10 402 Wanders (1976) Lithophyllum sp. Coral reef, Curacao 0.5–3 m 1.10 402 Wanders (1976) Neogoniolithon solubile Coral reef, Curacao 0.5–3 m 1.40 511 Wanders (1976) Melobesioid species Waikiki reef, Hawaii, USA 1.50 548 Littler (1973) Mainly Neogoniolithon frutescens Coral reef, Mooria, Tahiti 0.75 m 2.00 730 Sournia (1976) Porolithon onkodes Hawaiian Reef, USA 5 m 2.20 803 Littler and Doty (1975) Porolithon gardineri Hawaiian Reef, USA 5 m 2.40 876 Littler and Doty (1975) Corallina elongata Marseille, France 5 m 2.50 912 El Haïkali et al. (2004) Hydrolithon reinboldii Waikiki reef, Hawaii, USA 2.60 949 Littler (1973) Neogoniolithon conicum Lab. Lizard Island, Australia 0–18 m 0.6–4.65 219–1697 Chisholm (2003) Hydrolithon reinboldii Lab. Lizard Island, Australia 0–6 m 1.6–3.8 584–1387 Chisholm (2003) Neogoniolithon brassica-florida Lab. Lizard Island, Australia 0–6 m 2.45–3.35 894–1223 Chisholm (2003) Neogoniolithon conicum In situ Lizard Island, Australia 0–18 m 0.85–5.9 310–2154 Chisholm (2003) Neogoniolithon brassica-florida In situ Lizard Island, Australia 0–6 m 2.15–4.7 785–1716 Chisholm (2003) Hydrolithon onkodes In situ Lizard Island, Australia 0–3 m 1.75–6.55 639–2391 Chisholm (2003) Hydrolithon reinboldii In situ Lizard Island, Australia 3–6 m 4.15–4.35 1515–1588 Chisholm (2003) Hydrolithon onkodes Lab. Lizard Island, Australia 0–3 m 4.01–6.05 1464–2208 Chisholm (2003) Free-living algae 173 This study (n= 4) Nongeniculate corallines San Salvador Island, Bahamas 76 m 0.15 55 Littler et al. (1991) Maerl beds Bay of Brest, France 0.3–7.9 m 0.38 138 Martin et al. (2005) Lithophyllum sp. San Salvador Island, Bahamas 76 m 0.57 208 Littler et al. (1991) Lithothamnion corallioides Bay of Brest, France 1–10 m 10–600 Martin et al. (2006) 3 Processes and metabolism While coralline algae are slow growing, their high abundance and spatial distribution indicate their production is likely important (Johansen, 1981) and they are major contributors to the carbon and carbonate cycles of coastal environments (Martin et al., 2013a). Organic production relates to the photosynthetic capacity of coralline algae, while inorganic production relates to the calcium carbonate production (Johansen, 1981). 3.1 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 worldwide dispersal, corallines can contribute significantly to the total marine primary production (Roberts et al., 2002). Production of one mole of organic material (photosynthesis) decreases dissolved inorganic carbon (DIC) by one mole: CO2+H2O→ CH2O +O2. (R1) Primary production also decreases pCO2, however the magnitude of these changes depends on the equilibrium constants (Johansen, 1981). Respiration increases both DIC and pCO2 (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 Biogeosciences, 12, 6429–6441, 2015 www.biogeosciences.net/12/6429/2015/ L. H. van der Heijden and N. A. Kamenos: Calculating the global contribution of coralline algae 6433 Table 2. The global average production rates of autotrophic coastal communities. Macroalgae in Gattuso et al. (1998) were macrophytedominated. Macrophytobenthic communities in Charpy-Roubaud and Sournia (1990) included brown algae, seagrasses, mangroves and salt marshes. Community Production rate References (g C m−2 d−1) (g C m−2 yr−1) Coralline algae (average) 0.9 329 This study (n= 39) Free-living algae 0.15–0.83 173 This study (n= 4) Crustose coralline algae 0.07–5 370 This study (n= 35) 0.9–5 Chisholm (2003) Benthic fleshy algae 0.1–4 Larkum (1983) Turf algae 1–6 Larkum (1983) Mangroves 221 Duarte et al. (2005) 1081 Gattuso et al. (1998) Salt marshes 1585 Duarte et al. (2005) 210 Gattuso et al. (1998) Seagrasses 1–7L 1211D L =Larkum (1983) D =Duarte et al. (2005) 502 Ranwell (1966); Kirby and Gosselink (1976); Odum (1974); Turner (1976); Thayer and Adams (1975); Nienhuis and Bree (1977); Zieman (1975) Macroalgae 1587 Duarte et al. (2005) 222 Gattuso et al. (1998) Benthic diatoms 123 Cadee and Hegeman (1974) Coastal phytoplankton 0.1–0.5L 196W L =Larkum (1983) W =Woodwell et al. (1973); Cadee and Hegeman, (1974); Gieskes and Kraay (1975) Coral reefs 148 Duarte et al. (2005) 120 Gattuso et al. (1998) Macrophytobenthos 375 Charpy-Roubaud and Sournia (1990) is induced 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 underlying reef. 3.2 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 inorganicorganic production is high in coralline algae, compared to non-coralline seaweeds (Johansen, 1981). Precipitation of one mole CaCO3 decreases DIC by one mole and total alkalinity by two moles: Ca+ 2HCO−3 → CaCO3+H2O+CO2. (R2) For calcium carbonate to be deposited an alkaline environment is required, as well as high concentrations of calcium and carbonate (Johansen, 1981). Calcification of coralline algae occurs internally, compared to external calcification in corals and other invertebrates (Chisholm, 2003). The cellwalls of coralline algae are composed of calcium carbonate, and mainly consist of high Mg-calcite (HMC: > 4 % wt of MgCO3; Moberly, 1968; Kamenos et al., 2008; Basso, 2012). 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 animal-dominated, 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 the environmental conditions (Basso, 2012). Coralline algal calcification is indirectly affected by temperature, often over a season cycle, as well as by light limitation (Martin et al., 2006). 4 Potential global contribution of coralline algae to total carbon burial The shallow-water ocean environment (i.e. bays, estuaries, lagoons, banks, and continental shelves) accounts for 14– 30 % of the oceanic primary production, 80 % of organic material burial and ∼ 50 % of CaCO3 deposition (Gattuso et al., 1998). The total surface area of the coastal zone, the potential habitat for benthic coralline algae, is estimated between 0.45–49.4× 10 m (Charpy-Robaud and Sournia, 1990). The coastal area, that has depths ranging between 0 and 200 m covers 7.49 % of the world ocean, which corresponds to 27.123× 10 m (Menard and Smith, 1966). www.biogeosciences.net/12/6429/2015/ Biogeosciences, 12, 6429–6441, 2015 6434 L. H. van der Heijden and N. A. Kamenos: Calculating the global contribution of coralline algae Table 3. The total global production of different coastal communities compared to the total marine oceanic production. The macrophytoben-thic community in Charpy-Roubaud and Sournia (1990) included brown algae, seagrasses, mangroves and salt marshes. CommunityTotal global production References(in 109 t C yr−1) Coralline algae0.7 This study (n= 39)Microphytobenthic community0.34 Charpy-Roubaud and Sournia (1990)Algal beds and reefs community1.2 Whittaker and Likens (1973)Macrophytobenthic community2.55 Charpy-Roubaud and Sournia (1990)Phytoplankton community≥ 30 Charpy-Roubaud and Sournia (1990) Marine community48.5 Field et al. (1998) Charpy-Roubaud and Sournia (1990) suggest an area of6.8× 10 m, because the average benthic photic zone ofthe world is shallower than 200 m. Here we will use 33 % ofthe coastal zone, which is the part that receives enough lightfor photosynthesis (Gattuso et al., 2006) and thus assumingthat production mainly occurs in the top 66 m of the coastalzone. Because coralline algae usually attach to harder sub-strata (Bosence, 1983) the surface covered by coralline algae(Table S1) has to be taken into account. However, as thereare substrates (e.g. sandy substrata or other soft-bottom sub-strates) that are an unsuitable habitat for coralline algae, to beconservative, we have assumed only half of the estimated sur-face coverage percentages estimated above contain corallinealgae (CCA= 26.25 %, rhodoliths= 22.5 %, coralline algaemedian= 22.5 %). At present we have an incomplete knowl-edge of the real distribution of coralline algae, so we estimatea global production based on the following parameters: theproduction of coralline algae (median), the top 66 m globalcoastal zone and the surface of this coastal zone covered bycoralline algae (22.5 %). We use the median in/organic C pro-duction for coralline algae due to skewed data distribution(Zar, 1999) across available studies. 4.1 Global coralline algal organic C production Net primary production by coralline algae ranges widelyfrom 10 g C m yr by Lithothamnion corallioides inthe Bay of Brest, France (Martin et al., 2006) to2391 g C m yr by Hydrolithon onkodes at Lizard Is-land, Australia (Chisholm, 2003), giving a median produc-tion of 329 g C m yr (n= 39; Table 1) across depthsand locations. Global C production may thus be as high as0.7× 10 t C yr. The daily production of coralline algaecorresponds with the range of production of benthic fleshyalgae, turf algae, sand algae, phytoplankton, seagrasses andzooxanthellae (Table 2) and estimated yearly coralline algalproduction rate (329 g C m yr) is in the range of pro-duction by mangroves, salt marshes and seagrasses and ap-pears more productive than coastal phytoplankton, benthicdiatoms and coral reefs (Table 2). Payri (2000) observed thatthe annual production of a coralline algal communities corre-sponds to approximately one third of the production of sea-grass beds, which was also observed on the west-coast ofFrance with a production ratio of 3.12 (Martin et al., 2005).A production ratio of 1.5–3.7 is observed in this study whencompared to seagrass production rate studies (Table 2).The estimated production of free-living coralline algae(0.35× 10 t C yr) is in the range determined by otherstudies while the production for CCA (0.88× 10 t C yr)is slightly higher (Table 3). Thus, with a global oceanic pro-duction estimated at 48.5× 10 t C yr (Field et al., 1998)coralline algal production represent a measurable compo-nent. 4.2 Global inorganic coralline algal C production andaccumulation Studies focusing on coralline algae and calcium carbonate in-dicate a production range of 8–7400 g CaCO3 m−2 yr anda median of 900 g CaCO3 m −2 yr (Table 4). The globalnet calcium carbonate production using the previously es-timated surface coverage was 1.8× 10 t CaCO3 yr−1 forcoralline algae. Thus CaCO3 production by coralline algae of900 g CaCO3 m −2 yr lies within the range of coral reef cal-cite production of 75–4000 g CaCO3 m −2 yr (Canals andBallesteros, 1997) and is comparable with the coral reef pro-duction rate in the Late Holocene (1500 g CaCO3 m−2 yr;Milliman, 1993). Basso (2012) estimated an average pro-duction rate of 5 g CaCO3 m−2 yr for the coralline algaein the Mediterranean sea, however this included corallinealgae occurring below 100 m. Gattuso et al. (1998) sug-gested that communities in the coastal zone are responsiblefor more than 40 % (23× 10 t CaCO3 yr) of the total ma-rine calcium carbonate production. Thus the estimated cal-cite production by coralline algae is similar to the produc-tion of other coastal communities (e.g. coral reefs, banks andnon/carbonate shelves) and might represent a large fractionof the coastal and total ocean calcite production (Gattuso etal., 1998).Using average production rates for free-living algaeand CCA a net inorganic production was estimated forthese two groups. The net inorganic production for freeBiogeosciences, 12, 6429–6441, 2015www.biogeosciences.net/12/6429/2015/ L. H. van der Heijden and N. A. Kamenos: Calculating the global contribution of coralline algae6435 Table 4. Median net calcium carbonate production by coralline algae. Bracchi and Basso (2012) includes Lithophylloids, Canals and Balles-teros (1997) includes Peysonellia. SpeciesLocationDepth CaCO3 production Reference(g CaCO3 m −2 yr−1) Crustose coralline algae1225 This study (n= 24) Epiphyte corallines on seagrassMallorca-Menorca shelf, Mediterranean.0–35 m68 Canals and Ballesteros (1997) MesophyllumBarbadosfringing reef167 Stearn et al. (1977)Coralligenous build-ups + coralline species Mallorca-Menorca shelf, Mediterranean. 70–90 m170 Canals and Ballesteros (1997)Crustose coralline algaeUva Island, Panamareef flat190 Eakin (1996)Neogoniolithon brassica-florida+ geniculate Mallorca-Menorca shelf, Mediterranean.0–10 m289 Canals and Ballesteros (1997) Lithophyllum cabiochaeNW Mediterranean25 m292 Martin and Gattuso (2009) Lithophyllum incrustansSouth West Wales, United Kingdom intertidal pools379 Edyvean and Ford (1987)Epiphyte corallines on seagrassShark Bay, western Australia10 m500 Walker and Woelkerling (1988) Neogoniolithon conicumLizard Island, Australia0–18 m300–1550 Chisholm (2000) Hydrolithon reinboldiiLizard Island, Australia3–6 m910–1240 Chisholm (2000) Porolithon conicumLizard Island, Australia0–18 m318–1862 Chisholm (1988) NeogoniolithonBarbadosfringing reef1225 Stearn et al. (1977) Hydrolithon reinboldiiLizard Island, Australia3–6 m1035–1512 Chisholm (1988) LithophyllumBarbadosfringing reef1355 Stearn et al. (1977) Neogoniolithon brassica-floridaLizard Island, Australia0–6 m1200–2070 Chisholm (2000) Hydrolithon onkodesIshigaki Is (Ryukyu Is)upper fore reef2044 Matsuda (1989) Hydrolithon onkodesLizard Island, Australia0–3 m820–3310 Chisholm (2000) Porolithon onkodesPenguin Bank, Hawaii40–100 m2100 Agegian et al. (1988) Neogoniolithon foslieiLizard Island, Australia0–6 m1542–2815 Chisholm (1988) Porolithon onkodesLizard Island, Australia0–6 m947–3599 Chisholm (1988) PorolithonBarbadosfringing reef2378 Stearn et al. (1977) Coralline pavementOne Tree Island, Australia0–1 m4000 Kinsey (1985) Corallina elongataMarseille, France0.5–1 m5037 El Haïkali et al. (2004) Porolithon onkodesRangiroa, Polynesiareef flat7400 Payri (2000) Free-living algae187 This study (n= 14) mainly Lithothamnion spp.Pontian Islands shelf, west Meditte.70–100 m8 Bracchi and Basso (2012) mainly Lithothamnion spp.Pontian Islands shelf, west Meditte.40–70 m32 Bracchi and Basso (2012) Lithothamnion coralliodesCilento shelf, west Mediterranean47 m91 Savini et al. (2012)Rhodolith bedArvoredo Island, southern Brazil7–20 m55–136 Gherardi (2004) Lithothamnion corallioidesMannin Bay, Ireland0–10 m29–64 Bosence and Wilson (2003) Lithothamnion corallioidesGalway, Ireland< 10 m88–164 Bosence (1980) Phymatolithon calcareumMannin Bay, Ireland0–10 m79–249 Bosence and Wilson (2003) Phymalithon calcareum maerlMallorca-Menorca shelf, Mediterranean. 40–85 m210 Canals and Ballesteros (1997) Phymatolithon calcareumGalway, Ireland< 10 m79–422 Bosence (1980) Lithothamnion glacialeTroms, Norway18 m420–630 Freiwald and Henrich (1994) Lithothamnion coralliodesBay of Brest, France0–10 m876 Potin et al. (1990) Rhodolith bedAbrolhos shelf, Brazil20–110 m1000 Amado-Filho et al. (2012) Lithothamnion glacialeTroms, Norway7 m895–1432 Freiwald and Henrich (1994) Lithothamnion coralliodesBay of Brest, France1–10 m145–3100 Martin et al. (2006) Table 5. Accumulation rates of free-living coralline algae. Coralline algae in Bosence (1985) were predominantly Neogoniolithon species. SpeciesLocationCaCO3 accumulation Reference(mm kyr−1) Rhodolith (maerl)Troms district, Norway1400 Freiwald (1998)Mixed coralline algae Troms district, Norway900 Freiwald (1998)Coralline algaeOrkney Islands, Scotland80 Farrow et al. (1984)Branched coralline algae Tavernier Key, Florida, USA450 Bosence (1985) Rhodolith (maerl)St Mawes Bank, Falmouth, UK500 Bosence (1980) living algae was 22 g C-inorganic m yr and 150 g C-inorganic m yr for CCA. Thus net inorganic produc-tion by coralline algae of 108 g C-inorganic m yr andnet organic production of 330 g C-organic m yr gives aPIC : POC ratio of 0.33 (PIC is the particular inorganic car-bon and POC the particular organic carbon). The PIC : POCratio for free-living algae was 0.13 and 0.40 for the CCA.Significantly, a similar PIC : POC range of ratios of 0.23-0.29was also observed for coccolithophores (Engel et al., 2005). www.biogeosciences.net/12/6429/2015/Biogeosciences, 12, 6429–6441, 2015 6436L. H. van der Heijden and N. A. Kamenos: Calculating the global contribution of coralline algae 4.3 Global carbon accumulation The long-term removal of C requires the fixed carbon to re-main stored for 100–1000 years (Gattuso et al., 1998). Theglobal long-term deposition rate of free-living coralline al-gae is 500 mm kyr (Table 5) and the accumulation ratesrange from 80 to 1400 mm kyr for temperate (OrkneyIsland, Scotland) to polar (Tromsø district, Norway) sys-tems. The calcium carbonate production by free-livingalgae (187 g CaCO3 m −2 yr) with a calcite density of2.71 g cm (DeFoe and Compton, 1925) corresponds to asediment accretion of 70 mm kyr, while for CCA this cor-responds to a sediment accretion of 450 mm kyr. Giventhe accretion rate of 500 mm kyr, the preservation poten-tial of coralline algae would be 64 %. This is consistent withthe empirically calculated calcium carbonate preservation of60 % (Milliman, 1993). However, if the preservation of CCAis excluded because of the lack of available accretion rates,and heavy grazing (Steneck, 1986), the preservation potentialfor this morphotype would be 14 %. As the complete preser-vation potential for coralline algae still requires further refin-ing, the potential total carbon burial is estimated based on thesum of total organic production and the inorganic production.The estimated potential total burial for the free-living algaewas 0.4× 10 and 1.2× 10 t C yr for CCA giving a po-tential total carbon burial of 1.6× 10 t C yr for corallinealgae. 5 Future prospects: ocean acidification and risingtemperature Increasing atmospheric pCO2 will increase DIC and shift theequilibrium of the carbonate system to higher CO2 and bi-carbonate ion-levels, lower carbonate ion concentration andlower pH (Feely et al., 2009). Coralline algae may be vulner-able to the warming and lowering sea water pH of sea water,caused by recent increases in anthropogenic CO2 (Kleypaset al., 2006); the sensitivity of algae is of widespread impor-tance and it has generated several recent reviews which findcoralline algae may show mixed response to global change(Nelson et al., 2009; Koch et al., 2012; Brodie et al., 2014;McCoy and Kamenos, 2015). For example, high pCO2 con-ditions negatively affect community growth (Jokiel et al.,2008; Hofmann et al., 2012; Ragazzola et al., 2012), recruit-ment (Kuffner et al., 2008), calcification (Anthony et al.,2008; Gao and Zheng, 2010), size and abundance (Kuffneret al., 2008; Hall-Spencer et al., 2008; Porzio et al., 2011;Kroeker et al., 2013; McCoy and Ragazzola, 2014; Don-narumma et al., 2014), as well as epithelial integrity (Bur-dett et al., 2012). Conversely, increased atmospheric pCO2is expected to have a positive impact on the organic produc-tion and growth of algae due to increased pCO2 availability(Hendriks et al., 2010). For example, Semesi et al. (2009) ob-served an increase in photosynthetic rates of coralline algaewith a rising pCO2 of seawater, however, whether this alsotranslates to their accretion at longer timescales is still notclear.The HMC cell-walls of coralline algae, containing 7.7–28.8 % MgCO3, play a crucial role in their response to theincreased temperature and acidification of seawater (Basso,2012; Kamenos et al., 2013). Biogenic HMC cell-walls, con-taining > 8–12 % MgCO3, have a high solubility and are sen-sitive to ocean acidification (Andersson et al., 2008). Despitethis, there is evidence that they can continue to calcify in el-evated pCO2 (Kamenos et al., 2013; Martin et al., 2013b;Diaz-Pulido et al., 2014) but with altered skeletal integrity(Ragazzola et al., 2012; Kamenos et al., 2013; McCoy andRagazzola, 2014). Overall it is expected that any decreasingabundance and growth of coralline algae may have knock-onconsequences for worldwide coastal ecosystems (Johansen,1981; Martin and Gattuso, 2009; Basso, 2012).