Ocean acidification and seaweed reproduction: Increased CO 2 ameliorates the negative effect of lowered pH on meiospore germination in the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae)

Global Change Biology

Volumn 18, Issue 3, 2012, Pages 854-864

  Roleda, Michael Y ^a   Morris, Jaz N ^a   McGraw, Christina M ^a,b   Hurd, Catriona L ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b CLARK UNIVERSITY   (United States)

Author keywords

Early life history stages; Gametophyte; Macroalgae; Meiospore; Ocean acidification; PCO 2; Seaweed; Sex ratio

Indexed keywords

ACIDIFICATION; DISSOLVED INORGANIC CARBON; GAMETOPHYTE; GERMINATION; MACROALGA; REPRODUCTIVE STRATEGY; SEAWEED; SEX RATIO; TROPHIC LEVEL; ULTRAVIOLET B RADIATION;

LAMINARIALES; MACROCYSTIS; MACROCYSTIS PYRIFERA; PHAEOPHYCEAE;

EID: 84857141516     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/j.1365-2486.2011.02594.x     Document Type: Article

References (65)

1. Amsler CD, Neushul M (1991) Photosynthetic physiology and chemical composition of spores of the kelps, Macrocystis pyrifera, Nereocystis luetkeana, Laminaria farlowii, and Pterygophora californica (Phaeophyceae). Journal of Phycology, 27, 26-34.
2. Anthony KRN, Maynard JA, Diaz-Pulido G, Mumby PJ, Marshalls PA, Cao L, Hoegh-Guldberg O (2011) Ocean acidification and warming will lower reef resilience. Global Change Biology, 17, 1798-1808.
3. Beardall J, Beer S, Raven JA (1998) Biodiversity of marine plants in an era of climate change: some predictions based on physiological performance. Botanica Marina, 41, 113-123.
4. Borowitzka MA, Larkum AWD (1986) Reef algae. Oceanus, 29, 49-54.
5. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Science, 425, 365.
6. Carney LT, Edwards MS (2006) Cryptic processes in the sea: a review of delayed development in the microscopic stages of marine macroalgae. Algae, 21, 161-168.
7. 2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forest. Proceedings of the Royal Society B-Biological Sciences, 227, 1409-1415.
8. Cornwall CE, Hepburn CD, Pritchard D, Currie KI, McGraw CM, Hunter KA, Hurd CL (2011) Carbon use-strategies in macroalgae: differential responses to lowered pH and implications for ocean acidification. Journal of Phycology, doi: 10.1111/j.1529-8817.2011.01085.x.
9. 2 over a subantarctic Macrocystis kelp bed. Polar Biology, 23, 706-716.
10. 2 and DIC in the sub-Antarctic coastal area. Estuarine, Coastal and Shelf Science, 81, 114-122.
11. Dickson AG, Millero FJ (1987) A comparison of the equilibrium-constants for the dissociation of carbonic-acid in seawater media. Deep-Sea Research Part A-Oceanographic Research Papers, 34, 1733-1743.
12. Dickson AG, Riley JP (1978) The effect of analytical error on the evaluation of the components of the aquatic carbon-dioxide system. Marine Chemistry, 6, 77-85.
13. 2 measurements. PICES Special Publication, 3, 191.
14. 2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis. Marine Ecology Progress Series, 373, 285-294.
15. Edwards MS, Estes JA (2006) Catastrophe, recovery and range limitation in NE Pacific kelp forests: a large-scale perspective. Marine Ecology Progress Series, 320, 79-87.
16. 3 system in the oceans. Science, 305, 362-366.
17. Fukuda S, Suzuki I, Hama T, Shiraiwa Y (2011) Compensatory response of the unicellular-calcifying alga Emiliania huxleyi (Coccolithophoridales, Haptophyta) to ocean acidification. Journal of Oceanography, 67, 17-25.
18. Funano T (1983) The ecology of Laminaria religiosa Miyabe. I. The life history and alternation of nuclear phases of Laminaria religiosa, and the physiological ecology of the gametophytes and the embryonal sporophytes. Hokusui-Shiho, 25, 61-109.
19. Gao KS, Zheng YQ (2010) Combined effects of ocean acidification and solar UV radiation on photosynthesis, growth, pigmentation and calcification of the coralline alga Corallina sessilis (Rhodophyta). Global Change Biology, 16, 2388-2398.
20. 2 concentration. Journal of Applied Phycology, 3, 355-362.
21. 2. Marine Biology, 117, 129-132.
22. 2] of the past. New Phytologist, 188, 674-695.
23. Gosselin LA, Jones LA (2010) Effects of solar radiation on barnacle settlement, early post-settlement mortality and community development in the intertidal zone. Marine Ecology Progress Series, 407, 149-158.
24. Graham MH, Vásquez JA, Buschmann AH (2007) Global ecology of the giant kelp Macrocystis: from ecotypes to ecosystems. Oceanography and Marine Biology: An Annual Review, 45, 39-88.
25. Hall-Spencer J, Rodolfo-Metalpa R, Martin S et al. (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature, 454, 96-99.
26. Harrison PJ, Hurd CL (2001) Nutrient physiology of seaweeds: application of concepts to aquaculture. Cahiers de Biologie Marine, 42, 71-82.
27. Hedley J (2009) Vidana 1.0.1 Beta. Availabel at: (accessed 11 October 2011).
28. Henríquez LA, Buschmann AH, Maldonado MA, Graham MH, Hernandez-Gonzalez MC, Pereda SV, Bodadilla MI (2011) Grazing on giant kelp microscopic phases and the recruitment success of annual populations of Macrocystis pyrifera (Laminariales, Phaeophyta) in Southern Chile. Journal of Phycology, 47, 252-258.
29. 2 ocean. Global Change Biology, 17, 2488-2497.
30. Hinga KR (2002) Effects of pH on coastal marine phytoplankton. Marine Ecology Progress Series, 238, 281-300.
31. Hoegh-Guldberg O, Mumby PJ, Hooten AJ et al. (2007) Coral reefs under rapid climate change and ocean acidification. Science, 318, 1737-1742.
32. 2. Available at: (accessed 5 October 2011).
33. Hurd CL, Hepburn CD, Currie KI, Raven JA, Hunter KA (2009) Testing the effects of ocean acidification on algal metabolism: considerations for experimental designs. Journal of Phycology, 45, 1236-1251.
34. nd century ocean acidification: a mechanism for differential susceptibility? Global Change Biology, 17, 3254-3262.
35. IPCC (2007) Climate Change 2007: The Physical Science Basis. Summary for Policymakers. Contribution of Working Group I to the Fourth Assessment Report. The International Panel on Climate Change. Availabe at: (accessed 23 November 2011).
36. Johnston AM, Maberly SC, Raven JA (1992) The acquisition of inorganic carbon by four red macroalgae. Oecologia, 92, 317-326.
37. Kawachi M, Noël M-H (2005) Sterilization and sterile technique. In: Algal Culturing Techniques (ed Andersen RA), pp. 65-81. Elsevier, London.
38. 2 vent for ocean acidification studies. Estuarine, Coastal and Shelf Science, 94, 129-137.
39. 2 on the seaweed Lomentaria articulata. Plant, Cell and Environment, 22, 1303-1310.
40. Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS, Mackenzie FT (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nature Geoscience, 1, 114-117.
41. Lee JA, Brinkhuis BH (1988) Seasonal light and temperature interaction effects on development of Laminaria saccharina (Phaeophyta) gametophytes and juvenile sporophytes. Journal of Phycology, 24, 181-191.
42. Mann KH (1973) Seaweeds: their productivity and strategy for growth. Science, 182, 975-981.
43. Martin S, Gattuso JP (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Global Change Biology, 15, 2089-2100.
44. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography, 18, 897-907.
45. Nelson WA (2005) Life history and growth in culture of the endemic New Zealand kelp Lessonia variegata J. Agardh in response to differing regimes of temperature, photoperiod and light. Journal of Applied Phycology, 17, 23-28.
46. North WJ, Hubbs CL (1968) Utilization of kelp-bed resources in Southern California. Fish Bulletin, 139, 1-264. Available at: (accessed 18 November 2011).
47. North WJ, Jackson GA, Manley SL (1986) Macrocystis and its environment, knowns and unknowns. Aquatic Botany, 26, 9-26.
48. Oppliger LV, Correa JA, Faugeron S, Beltrán J, Tellier F, Valero M, Destombe C (2011) Sex ratio variation in the Lessonia nigrescens complex (Laminariales, Phaeophyceae): effect of latitude, temperature, and marginality. Journal of Phycology, 47, 5-12.
49. Porzio L, Buia MC, Hall-Spencer JM (2011) Effects of ocean acidification on macroalgal communities. Journal of Experimental Marine Biology and Ecology, 400, 278-287.
50. Raffo MP, Eyras MC, Iribarne OO (2009) The invasion of Undaria pinnatifida to a Macrocystis pyrifera kelp in Patagonia (Argentina, south-west Atlantic). Journal of the Marine Biological Association of the United Kingdom, 89, 1571-1580.
51. Raven JA (1997) Inorganic carbon acquisition by marine autotrophs. Advances in Botanical Research, 27, 85-209.
52. Raven JA, Cockell CS, La Rocha CL (2008) The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philosophical Transactions of the Royal Society B-Biological Sciences, 363, 2641-2650.
53. Readdie MD (2003) Giant Kelp Macrocystis pyrifera (C. Agardh). Available at: (accessed 28 October 2011).
54. Riebesell U, Fabry VJ, Hansson L, Gattuso J-P (2010) Guide to Best Practices for Ocean Acidification Research and Data Reporting. Publications Office of the European Union, Belgium.
55. Roleda MY, Wiencke C, Hanelt D, Bischof K (2007) Sensitivity of the early life history stages of macroalgae from the Northern Hemisphere to ultraviolet radiation. Photochemistry and Photobiology, 83, 851-862.
56. Roleda MY, Lüder UH, Wiencke C (2010) UV-susceptibility of zoospores of the brown macroalga Laminaria digitata from Spitsbergen. Polar Biology, 33, 577-588.
57. Royal Society (2005) Ocean Acidification due to Increasing Atmospheric Carbon Dioxide. Policy document 12/05 Royal Society, London. The Clyvedon Press Ltd, Cardiff.
58. 2 and nutrient-driven change in subtidal rocky habitats. Global Change Biology, 15, 2153-2162.
59. 2 modifies the influence of light in shaping subtidal habitat. Journal of Phycology, 47, 744-752.
60. 2 affect calcification and photosynthesis in the tropical coralline alga, Hydrolithon sp. (Rhodophyta). Estuarine Coastal and Shelf Science, 84, 337-341.
61. Sorokin C (1962) Inhibition of cell division by carbon dioxide. Nature, 194, 496-497.
62. Sorokin C (1964) Effects of acidity on cell division. Experimental Cell Research, 27, 583-584.
63. Tellier F, Tapia J, Faugeron S, Destombe C, Valero M (2011) The Lessonia nigrescens species complex (Laminariales, Phaeophyceae) shows strict parapatry and complete reproductive isolation in a secondary contact zone. Journal of Phycology, 47, 894-903.
64. Uller T, Pen I, Wapstra E, Beukeboom LW, Komdeur J (2007) The evolution of sex ratios and sex-determining systems. Trends in Ecology and Evolution, 22, 292-297.
65. 2 concentrations on emersed photosynthesis in Porphyra haitanensis (Bangiales, Rhodophyta), a species farmed in China. European Journal of Phycology, 37, 587-592.