Ocean acidification effects on calcifying macroalgae

Aquatic Biology

Volumn 22, Issue , 2014, Pages 261-279

  Hofmann, Laurie C ^a   Bischof, Kai ^a  

^a UNIVERSITY OF BREMEN   (Germany)

Author keywords

Benthic communities; Calcification; Eutrophication; Macroalgae; Ocean acidification

Indexed keywords

ALGAE;

EID: 84926300805     PISSN: 18647782     EISSN: 18647790     Source Type: Journal    
DOI: 10.3354/ab00581     Document Type: Review

References (135)

1. Adey WH (1998) Coral reefs: algal structured and mediated ecosystems in shallow, turbulent, alkaline waters. J Phycol 34: 393-406.
2. Al-Horani FA, Al-Moghrabi SM, De Beer D (2003) The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142: 419-426.
3. Albright R (2011) Reviewing the effects of ocean acidification on sexual reproduction and early life history stages of reef-building corals. J Mar Biol 2011: 1-14.
4. Albright R, Mason B, Miller M, Langdon C (2010) Ocean acidification compromises recruitment success of the threatened Caribbean coral Acropora palmata. Proc Natl Acad Sci USA 107: 20400-20404.
5. Andersson AJ, Mackenzie FT, Bates NR (2008) Life on the margin: implications of ocean acidification on Mgcalcite, high latitude and cold-water marine calcifiers. Mar Ecol Prog Ser 373: 265-273.
6. Andersson AJ, Kuffner IB, Mackenzie FT, Jokiel PL, Rodgers KS, Tan A (2009) Net loss of CaCO3 from coral reef communities due to human induced seawater acidification. Biogeosciences Discuss 6: 2163-2182.
7. Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh- Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci USA 105: 17442-17446.
8. Axelsson L, Uusitalo J (1988) Carbon acquisition strategies for marine macroalgae. Mar Biol 97: 295-300.
9. Axelsson L, Ryberg H, Beer S (1995) Two modes of bicarbonate utilization in the marine green macroalga Ulva lactuca. Plant Cell Environ 18: 439-445.
10. Bilan MI, Usov AI (2001) Polysaccharides of calcareous algae and their effect on the calcification process. Russ J Bioorg Chem 27: 2-16.
11. Borowitzka MA (1981) Photosynthesis and calcification in the articulated coralline red algae Amphiroa anceps and A. foliacea. Mar Biol 62: 17-23.
12. Borowitzka MA (1984) Calcification in aquatic plants. Plant Cell Environ 7: 457-466.
13. Borowitzka MA, Larkum AWD (1976a) Calcification in the green alga Halimeda. II. The exchange of Ca2+ and the occurrence of age gradients in calcification and photosynthesis. J Exp Bot 27: 864-878.
14. Borowitzka MA, Larkum AWD (1976b) Calcification in the green alga Halimeda. III. The sources of inorganic carbon for photosynthesis and calcification and a model of the mechanism of calcification. J Exp Bot 27: 879-889.
15. Borowitzka MA, Larkum AWD (1977) Calcification in the green alga Halimeda. I. An ultrastructure study of thallus development. J Phycol 13: 6-16.
16. Borowitzka MA, Larkum AWD (1987) Calcification in algae: mechanisms and the role of metabolism. Crit Rev Plant Sci 6: 1-4.
17. Büdenbender J, Riebesell U, Form A (2011) Calcification of the Arctic coralline red algae Lithothamnion glaciale in response to elevated CO2. Mar Ecol Prog Ser 441: 79-87.
18. Burdett HL, Aloisio E, Calosi P, Findlay HS, Widdicombe S, Hatton AD, Kamenos NA (2012) The effect of chronic and acute low pH on the intracellular DMSP production and epithelial cell morphology of red coralline algae. Mar Biol Res 8: 756-763.
19. Burdett HL, Donohue PJC, Hatton AD, Alwany MA, Kamenos NA (2013) Spatiotemporal variability of dimethyl sulphoniopropionate on a fringing coral reef: the role of reefal carbonate chemistry and environmental variability. PLoS ONE 8: e64651.
20. Campbell JE (2012) The effects of carbon dioxide fertilization on the ecology of tropical seagrass communities. PhD dissertation, Florida International University, Miami, FL.
21. 2 do not exhibit a tipping point. Limnol Oceanogr 58: 388-398.
22. Cornwall CE, Hepburn CD, Pritchard D, Currie KI, McGraw CM, Hunter KA, Hurd CL (2012) Carbon-use strategies in macroalgae: differential responses to lowered pH and implications for ocean acidification. J Phycol 48: 137-144.
23. Cornwall CE, Hepburn CD, Pilditch CA, Hurd CL (2013) Concentration boundary layers around complex assemblages of macroalgae: implications for the effects of ocean acidification on understory coralline algae. Limnol Oceanogr 58: 121-130.
24. Cumani F, Bradassi F, Di Pascoli A, Bressan G (2010) Marine acidification effects on reproduction and growth rates of Corallinaceae spores (Rhodophyta). Rapp Comm Int Mer Medit 39: 735.
25. de Beer C, Larkum AWD (2001) Photosynthesis and calcification in the calcifying algae Halimeda discoidea studied with microsensors. Plant Cell Environ 24: 1209-1217.
26. Delgado O, Lapointe BE (1994) Nutrient-limited productivity of calcareous versus fleshy macroalgae in a eutrophic, carbonate-rich tropical marine environment. Coral Reefs 13: 151-159.
27. Diaz-Pulido G, Nash MC, Anthony KRN, Bender D, Opdyke BN, Reyes-Nivia C, Troitzsch U (2014) Greenhouse conditions induce mineralogical changes and dolomite accumulation in coralline algae on tropical reefs. Nat Commun 5: 3310.
28. Digby PSB (1977a) Growth and calcification in the coralline algae, Clathromorphum circumscriptum and Corallina officinalis, and the significance of pH in relation to precipitation. J Mar Biol Assoc UK 57: 1095-1110.
29. Digby PSB (1977b) Photosynthesis and respiration in the coralline algae, Clathromorphum circumscriptum and Corallina officinalis and the metabolic basis of calcification. J Mar Biol Assoc UK 57: 1111-1112.
30. Dijoux L, Verbruggen H, Mattio L, Duong N, Payri C (2012) Diversity of Halimeda (Bryopsidales, Chlorophyta) in New Caledonia: a combined morphological and molecular study. J Phycol 48: 1465-1481.
31. Done TJ (1992) Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247: 121-132.
32. Drechsler Z, Beer S (1991) Utilization of inorganic carbon by Ulva lactuca. Plant Physiol 97: 1439-1444.
33. Edmunds PJ, Carpenter RC, Comeau S (2013) Understanding the threats of ocean acidification to coral reefs. Oceangraphy 26: 149-152.
34. 2 on physiology and skeletal mineralogy in a tidal pool coralline alga Corallina elongata. Mar Biol 160: 2103-2112.
35. Enríquez S, Rodríguez-Román A (2006) Effect of water flow on the photosynthesis of three marine macrophytes from a fringing-reef lagoon. Mar Ecol Prog Ser 323: 119-132.
36. Enríquez S, Méndez ER, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Oceanogr 50: 1025-1032.
37. Fabricius KE, Langdon C, Uthicke S, Humphrey C and others (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Chang 1: 165-169.
38. 2 enrichment. Mar Ecol Prog Ser 497: 87-92.
39. Gao K, Zheng Y (2010) Combined effects of ocean acidification and solar UV radiation on photosynthesis, growth, pigmentation and calcification of the coralline alga Corallina sessilis (Rhodophyta). Glob Change Biol 16: 2388-2398.
40. 2 concentrations. J Appl Phycol 3: 355-362.
41. 2 on growth and photosynthesis of the red algae Gracilaria sp. and G. chilensis. J Appl Phycol 5: 563-571.
42. Gao K, Helbling EW, Häder DP, Hutchins DA (2012) Responses of marine primary producers to interactions between ocean acidification, solar radiation, and warming. Mar Ecol Prog Ser 470: 167-189.
43. García-Sánchez MJ, Fernández JA, Niell X (1994) Effect of inorganic carbon supply on the photosynthetic physiology of Gracilaria tenuistipitata. Planta 194: 55-61.
44. Guinotte JM, Buddemeier RW, Kleypas JA (2003) Future coral reef habitat marginality: temporal and spatial effects of climate change in the Pacific basin. Coral Reefs 22: 551-558.
45. Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E and others (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454: 96-99.
46. Hay ME, Kappel QE, Fenical W (1994) Synergisms in plant defenses against herbivores: interactions of chemistry, calcification, and plant quality. Ecology 75: 1714-1726.
47. Hereu B (2006) Depletion of palatable algae by sea urchins and fishes in a Mediterranean subtidal community. Mar Ecol Prog Ser 313: 95-103.
48. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS and others (2007) Coral reefs under rapid climate change and ocean acidification. Science 318: 1737-1742.
49. 2 levels. Mar Ecol Prog Ser 464: 89-105.
50. 2 levels. Mar Biol 159: 783-792.
51. 2 levels affect the activity of nitrate reductase and carbonic anhydrase in the calcifying rhodophyte Corallina officinalis. J Exp Bot 64: 899-908.
52. Hofmann LC, Heiden J, Bischof K, Teichberg M (2014) Nutrient availability affects the response of the calcifying chlorophyte Halimeda opuntia (L.) J. V. Lamouroux to low pH. Planta 239: 231-242.
53. Hughes TP (1994) Catastrophes, phase shifts, and largescale degradation of a Caribbean coral reef. Science 265: 1547-1551.
54. Hurd CL, Cornwall CE, Currie K, Hepburn CD, McGraw CM, Hunter KA, Boyd P (2011) Metabolically induced pH fluctuations by some coastal calcifiers exceed projected 22nd century ocean acidification: a mechanisms for differential susceptibility? Glob Change Biol 17: 3254-3262.
55. 2 concentrations. Glob Change Biol 8: 831-840.
56. Israel A, Katz S, Dubinsky Z, Merrill JE, Friedlander M (1999) Photosynthetic inorganic carbon utilization and growth of Porphyra linearis (Rhodophyta). J Appl Phycol 11: 447-453.
57. James NP, Wray JL, Ginsburg RN (1988) Calcification of encrusting aragonitic algae (Peyssonneliaceae): implications for the origin of Late Paleozoic reefs and cements. J Sediment Res 58: 291-303.
58. Johnson MD, Carpenter RC (2012) Ocean acidification and warming decrease calcification in the crustose coralline alga Hydrolithon onkodes and increase susceptibility to grazing. J Exp Mar Biol Ecol 434-435: 94-101.
59. 2 gradients. Glob Change Biol 18: 2792-2803.
60. Johnson MD, Moriarty VW, Carpenter RC (2014) Acclimatization of the crustose coralline alga Porolithon onkodes to variable pCO2. PLoS ONE 9: e87678.
61. Jokiel PL, Rodgers KS, Kuffner IB, Andersson AJ, Cox EF, Mackenzie FT (2008) Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27: 473-483.
62. Kamenos NA, Burdett HL, Aloisio E, Findlay HS and others (2013) Coralline algal structure is more sensitive to rate, rather than the magnitude, of ocean acidification. Glob Change Biol 19: 3621-3628.
63. Kingsley RJ, Watabe N (1987) Role of carbonic anhydrase in calcification in the gorgonian Leptogorgia virgulata. J Exp Zool 241: 171-180.
64. Koch M, Bowes G, Ross C, Zhang X (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Change Biol 19: 103-132.
65. Kraft GT, Saunders GW, Abbott IA, Haroun RJ (2004) A uniquely calcified brown alga from Hawaii: Newhousia imricata gen. et sp. nov. (Dictyotales, Phaeophyceae). J Phycol 40: 383-394.
66. 2 and O2 on the seaweed Lomentaria articulata. Plant Cell Environ 22: 1303-1310.
67. Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS, Mackenzie FT (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geoscience 1: 114-117.
68. Langdon C, Takahashi T, Chipman D, Goddard J (2000) Effect of calcium carbonate saturation state on the calcification rate of an experimental reef. Global Biogeochem Cycles 14: 639-654.
69. 2 on the community metabolism of an experimental coral reef. Global Biogeochem Cycles 17: 1011, doi: 10.1029/2002GB001941.
70. Lapointe BE, Littler MM, Littler DS (1997) Macroalgal overgrowth of fringing coral reefs at Discovery Bay, Jamaica: bottom-up versus top-down control. Proc 8th Int Coral Reef Symp 1: 927-932.
71. 2 partial pressure controls the calcification rate of a coral community. Glob Change Biol 6: 329-334.
72. Lee D, Carpenter SJ (2001) Isotopic disequilibrium in marine calcareous algae. Chem Geol 172: 307-332.
73. Littler M (1976) Calcification and its role among the macroalgae. Micronesica 12: 27-41.
74. Martin S, Gattuso JP (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Change Biol 15: 2089-2100.
75. 2 and temperature. Ecol Evol 3: 676-693.
76. 2 hydroxylation generates protons for bicarbonate assimilation. Limnol Oceanogr 36: 619-628.
77. McConnaughey TA, Falk RH (1991) Calcium-proton exchange during algal calcification. Biol Bull 180: 185-195.
78. McConnaughey TA, Whelan JF (1997) Calcification generates protons for nutrient and bicarbonate uptake. Earth Sci Rev 42: 95-117.
79. McCulloch M, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Chang 2: 1-5.
80. Meehl GA, Stocker TF, Collins WD, Friedlingstein P and others (2007) Global climate projections. In: Solomon S, Qin D, Manning M, Chen Z and others (eds) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, p 747-845.
81. Mercado JM, Gordillo FJL, Figueroa FL, Niell FX (1998) External carbonic anhydrase and affinity for inorganic carbon in intertidal macroalgae. J Exp Mar Biol Ecol 221: 209-220.
82. 2 to increase the efficiency of photosynthetic carbon fixation? Plant Physiol 119: 9-16.
83. Moulin P, Andría JR, Axelsson L, Mercado JM (2011) Different mechanisms of inorganic carbon acquisition in red macroalgae (Rhodophyta) revealed by the use of TRIS buffer. Aquat Bot 95: 31-38.
84. Nash MC, Troitzsch U, Opdyke BN, Trafford JM, Russell BD, Kline DI (2011a) Biomineralization of dolomite and magnesite discovered in tropical coralline algae: a biological solution to the geological dolomite problem. Biogeosci Discuss 8: 5881-5906.
85. Nash MC, Troitzsch U, Opdyke BN, Trafford JM, Russell BD, Kline DI (2011b) First discovery of dolomite and magnesite in living coralline algae and its geobiological implications. Biogeosciences 8: 3331-3340.
86. Nash MC, Opdyke BN, Troitzsch U, Russell BD and others (2012) Dolomite-rich coralline algae in reefs resist dissolution in acidified conditions. Nat Clim Chang 3: 268-272.
87. Nelson WA (2009) Calcified macroalgae—critical to coastal ecosystems and vulnerable to change: a review. Mar Freshw Res 60: 787-801.
88. Noisette F, Egilsdottir H, Davoult D, Martin S (2013) Physiological responses of three temperate coralline algae from contrasting habitats to near-future ocean acidification. J Exp Mar Biol Ecol 448: 179-187.
89. Okazaki M, Pentecost A, Tanaka Y, Miyata M (1986) A study of calcium carbonate deposition in the genus Padina (Phaeophyceae, Dictyotales). Br Phycol J 21: 217-224.
90. Olabarria C, Arenas F, Viejo RM, Gestoso I and others (2013) Response of macroalgal assemblages from rockpools to climate change: effects of persistent increase in temperature and CO2. Oikos 122: 1065-1079.
91. Orr JC, Fabry VJ, Aumont O, Bopp L and others (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681-686.
92. Pennings SC, Svedberg J (1993) Does CaCO3 in food deter feeding by sea urchins? Mar Ecol Prog Ser 101: 163-167.
93. Porzio L, Buia MC, Hall-Spencer JM (2011) Effects of ocean acidification on macroalgal communities. J Exp Mar Biol Ecol 400: 278-287.
94. Price NN, Hamilton SL, Smith JE (2011) Species-specific consequences of ocean acidification for the calcareous tropical green algae Halimeda. Mar Ecol Prog Ser 440: 67-78.
95. Ragazzola F (2009) Carbon acquisition mechanisms in Corallina elongata Ellis & Solander and Corallina officinalis L. PhD dissertation, University of Pisa.
96. Ragazzola F, Foster LC, Form A, Anderson PS, Hansteen TH, Fietzke J (2012) Ocean acidification weakens the structural integrity of coralline algae. Glob Change Biol 18: 2804-2812.
97. Rahman MA, Oomori T, Uehara T (2008) Carbonic anhydrase in calcified endoskeleton: novel activity in biocalcification in alcyonarian. Mar Biotechnol 10: 31-38.
98. Raven JA (1997) Inorganic carbon acquisition by marine autotrophs. Adv Bot Res 27: 85-209.
99. Raven JA (2003) Inorganic carbon concentrating mechanisms in relation to the biology of algae. Photosynth Res 77: 155-171.
100. Raven JA, Johnston AM, Kübler JE, Korb R and others (2002) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29: 355-378.
101. Raven JA, Giordano M, Beardall J, Maberly SC (2012) Algal evolution in relation to atmospheric CO2: carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles. Philos Trans R Soc Lond B Biol Sci 367: 493-507.
102. Reyes-Nivia C, Diaz-Pulido G, Dove S (2014) Relative roles of endolithic algae and carbonate chemistry variability in the skeletal dissolution of crustose coralline algae. Biogeosci Discuss 11: 2993-3021.
103. Ries JB (2009) Effects of secular variation in seawater Mg/Ca ratio (calcite-aragonite seas) on CaCO3 sediment production by the calcareous algae Halimeda, Penicillus and Udoteaevidence from recent experiments and the geological record. Terra Nova 21: 323-339.
104. 2 world. J Exp Mar Biol Ecol 403: 54-64.
105. Ries JB (2011b) Acid ocean cover up. Nat Clim Chang 1: 294-295.
106. Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37: 1131-1134.
107. Robbins LL, Knorr PO, Hallock P (2009) Response of Halimeda to ocean acidification: field and laboratory evidence. Biogeosci Discuss 6: 4895-4918.
108. Rodolfo-Metalpa R, Houlbrèque F, Tambutté É, Boisson F and others (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nat Clim Chang 1: 308-312.
109. Roleda MY, Boyd PW, Hurd CL (2012) Before ocean acidification: calcifier chemistry lessons. J Phycol 48: 840-843.
110. 2 and nutrient-driven change in subtidal rocky habitats. Glob Change Biol 15: 2153-2162.
111. 2 modifies the influence of light in shaping subtidal habitat. J Phycol 47:744–752.
112. Sabine CL, Feely RA (2007) The oceanic sink for carbon dioxide. In: Reay D, Hewitt N, Grace J, Smith K (eds) Greenhouse gas sinks. CABI Publishing, Wallingford, p 31-49.
113. Sabine CL, Feely RA, Gruber N, Key RM and others (2004) The oceanic sink for anthropogenic CO2. Science 305: 367-371.
114. Sammarco PW (1982) Effects of grazing by Diadema antillarum Philippi (Echinodermata: Echinoidea) on algal diversity and community structure. J Exp Mar Biol Ecol 65: 83-105.
115. 2 affect calcification and photosynthesis in the tropical coralline alga, Hydrolithon sp. (Rhodophyta). Estuar Coast Shelf Sci 84: 337-341.
116. Siegenthaler U, Sarmiento JL (1993) Atmospheric carbon dioxide and the ocean. Nature 365: 119-125.
117. Sinutok S, Hill R, Doblin MA, Wuhrer R, Ralph PJ (2011) Warmer more acidic conditions cause decreased productivity and calcification in subtropical coral reef sediment- dwelling calcifiers. Limnol Oceanogr 56: 1200-1212.
118. Smith RG, Bidwell RG (1989) Mechanism of photosynthetic carbon dioxide uptake by the red macroalga, Chondrus crispus. Plant Physiol 89: 93-99.
119. Smith AD, Roth AA (1979) Effect of carbon dioxide concentration on calcification in the red coralline alga Bossiella orbigniana. Mar Biol 52: 217-225.
120. Stefels J (2000) Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J Sea Res 43: 183-197.
121. Steinacher M, Joos F, Frölicher TL, Plattner GK, Doney SC (2009) Imminent ocean acidification in the Arctic projected with the NCAR global coupled carbon cycleclimate model. Biogeosciences 6: 515-533.
122. Steneck RS (1983) Escalating herbivory and resulting adaptive trends in calcareous algal crusts. Paleobiology 9: 44-61.
123. Sültemeyer D (1998) Carbonic anhydrase in eukaryotic algae: characterization, regulation, and possible function during photosynthesis. Can J Bot 76: 962-972.
124. Tait LW (2014) Impacts of natural and manipulated variations in temperature, pH and light on photosynthetic parameters of coralline-kelp assemblages. J Exp Mar Biol Ecol 454: 1-8.
125. Tambutté S, Tambutté E, Zoccola D, Caminiti N and others (2007) Characterization and role of carbonic anhydrase in the calcification process of the azooxanthellate coral Tubastrea aurea. Mar Biol 151: 71-83.
126. Teichert S, Freiwald A (2013) Polar coralline algal CaCO3production rates correspond to intensity and duration of the solar radiation. Biogeosci Discuss 10: 14115-14140.
127. Teichberg M, Fricke A, Bischof K (2013) Increased physiological performance of the calcifying green macroalga Halimeda opuntia in response to experimental nutrient enrichment on a Caribbean coral reef. Aquat Bot 104: 25-33.
128. Terán E, Méndez ER, Enríquez S, Iglesias-Prieto R (2010) Multiple light scattering and absorption in reef-building corals. Appl Opt 49: 5032-5042.
129. Valiela I, McClelland J, Hauxwell J, Behr PJ, Hersh D, Foreman K (1997) Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences. Limnol Oceanogr 42: 1105-1118.
130. Van Alstyne KL, Houser LT (2003) Dimethylsulphide release during macroinvertebrate grazing and its role as an activated chemical defense. Mar Ecol Prog Ser 250: 175-181.
131. Van Alstyne KL, Wolfe GV, Freidenburg TL, Neill A, Hicken C (2001) Activated defense systems in marine macroalgae: evidence for an ecological role for DMSP cleavage. Mar Ecol Prog Ser 213: 53-65.
132. Verbruggen H, Kooistra WHCF (2004) Morphological characterization of lineages within the calcified tropical seaweed genus Halimeda (Bryopsidales, Chlorophyta). Eur J Phycol 39: 213-228.
133. 2 concentration on photosynthesis and growth of micro- and macro-algae. Sci China C Life Sci 51: 1144-1150.
134. Yildiz G, Hofmann LC, Bischof K, Dere (2013) Ultraviolet radiation modulates the physiological responses of the calcified rhodophyte Corallina officinalis to elevated CO2. Bot Mar 56: 161-168.
135. 2 on growth, photosynthesis and nitrogen metabolism in the economic brown seaweed, Hizikia fusiforme (Sargassaceae, Phaeophyta). Aquaculture 250: 726-735.