The impact of CO2 emission scenarios and nutrient enrichment on a common coral reef macroalga is modified by temporal effects

Journal of Phycology

Volumn 50, Issue 1, 2014, Pages 203-215

  Bender, Dorothea ^a   Diaz Pulido, Guillermo ^b   Dove, Sophie ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

Author keywords

Chnoospora implexa; Coral reef; Macroalgae; Nutrient enrichment; Ocean acidification; Season; Temperature

Indexed keywords

EID: 84894101980     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/jpy.12153     Document Type: Article

References (79)

1. 3 at high pH by the brown macroalga Laminaria saccharina. Eur. J. Phycol. 35:53-9.
2. Babcock, R. C., Bull, G. D., Harrison, P. L., Heyward, A. J., Oliver, J. K., Wallace, C. C. & Willis, B. L. 1986. Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef. Mar. Biol. 90:379-94.
3. 2-concentrating mechanisms in algae. Can. J. Bot. 76:1052-71.
4. Badger, M. R. & Collatz, G. J. 1977. Studies on the kinetic mechanism of ribulose-1, 5-bisphosphate carboxylase and oxygenase reactions, with particular reference to the effect of temperature on kinetic parameters. Carnegie Institute of Washington Yearbook. Carnegie Institute of Washington, Stanford, CA, pp. 355-61.
5. Badger, M. R., von Caemmerer, S., Ruuska, S. & Nakano, H. 2000. Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and RubisCO oxygenase. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355:1433-46.
6. Beardall, J., Beer, S. & Raven, J. A. 1998. Biodiversity of marine plants in an era of climate change: some predictions based on physiological performance. Bot. Mar. 41:113-24.
7. Bender, D., Diaz-Pulido, G. & Dove, S. 2012. Effects of macroalgae on corals recovering from disturbance. J. Exp. Mar. Biol. Ecol. 429:15-9.
8. Bird, K. T., Habig, C. & DeBusk, T. 1982. Nitrogen allocation and storage patterns in Gracilaria tikvahiae (Rhodophyta). J. Phycol. 18:344-8.
9. Birrell, C. L., McCook, L. J., Willis, B. & Diaz-Pulido, G. 2008. Effects of benthic algae on the replenishment of corals and the implications for the resilience of coral reefs. Oceanogr. Mar. Biol. Annu. Rev. 46:25-64.
10. Bohne, F. & Linden, H. 2002. Regulation of carotenoid biosynthesis genes in response to light in Chlamydomonas reinhardtii. BBA Gene Struct. Expr. 1579:26-34.
11. Chan, A., Lubarsky, K., Judy, K. & Fong, P. 2012. Nutrient addition increases consumption rates of tropical algae with different initial palatabilities. Mar. Ecol. Prog. Ser. 465:25-31.
12. Chapman, A. R. O. & Craigie, J. S. 1977. Seasonal growth in Laminaria longicruris: relations with dissolved inorganic nutrients and internal reserves of nitrogen. Mar. Biol. 40:197-205.
13. Cornwall, C. E., Hepburn, C. D., Pritchard, D., Currie, K. I., McGraw, C. M., Hunter, K. A. & Hurd, C. L. 2012. Carbon-use strategies in macroalgae: differential responses to lowered pH and implications for ocean acidification. J. Phycol. 48:137-44.
14. Crawley, A., Kline, D. I., Dunn, S., Anthony, K. R. N. & Dove, S. 2010. The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Glob. Change Biol. 16:851-63.
15. Dailer, M. L., Smith, J. E. & Smith, C. M. 2012. Responses of bloom forming and non-bloom forming macroalgae to nutrient enrichment in Hawai'i, USA. Harmful Algae 17:111-25.
16. Devlin, M., Waterhouse, J., Taylor, J. & Brodie, J. 2001. Flood Plumes in the Great Barrier Reef: Spatial and Temporal Patterns in Composition and Distribution. Great Barrier Reef Marine Park Authority, Townsville, Australia.
17. Diaz-Pulido, G. M. L. J. 2003. Relative roles of herbivory and nutrients in the recruitment of coral-reef seaweeds. Ecology 84:2026-33.
18. 2 enhances the competitive strength of seaweeds over corals. Ecol. Lett. 14:156-62.
19. Diaz-Pulido, G., McCook, L., Larkum, A., Lotze, H., Raven, J., Schaffelke, B., Smith, J. & Steneck, R. 2007. Vulnerability of macroalgae of the Great Barrier Reef to climate change, Chapter 7. In Johnson, J. & Marshall, P. [Eds.] Climate Change and the Great Barrier Reef: A Vulnerability Assessment. Great Barrier Reef Marine Park Authority and the Australian Greenhouse Office, Department of the Environment and Water Resources, Townsville, Australia, pp. 153-92.
20. Done, T. J. 1992. Phase shifts in coral reef communities and their ecological significance. Hydrobiologia 247:121-32.
21. Dove, S., Ortiz, J. C., Enriquez, S., Fine, M., Fisher, P., Iglesias-Prieto, R., Thornhill, D. & Hoegh-Guldberg, O. 2006. Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnol. Oceanogr. 51:1149-58.
22. Fang, J., Mello-Athayde, M., Schönberg, C., Kline, D., Hoegh-Guldberg, O. & Dove, S. 2013. Sponge biomass and bioerosion rates increase under ocean warming and acidification. Glob. Change Biol. 19:3581-91.
23. Furnas, M. J. 2003. Catchments and Corals: Terrestrial Runoff to the Great Barrier Reef. Australian Institute of Marine Science & CRC Reef Research Centre, Townsville, QLD, Australia, 334 pp.
24. 2 affect reef octocorals? Eco. Evol. 3:465-73.
25. 2 and bicarbonate as inorganic carbon sources for triacylglycerol and starch accumulation in Chlamydomonas reinhardtii. Biotechnol. Bioeng. 110:87-96.
26. Genty, B., Briantais, J. M. & Baker, N. R. 1989. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 990:87-92.
27. Gerloff, G. C. & Krombholz, P. H. 1966. Tissue analysis as a measure of nutrient availability for the growth of angiosperm aquatic plants. Limnol. Oceanogr. 11:529-37.
28. 2 level in the nitrophilic seaweed Ulva rigida C. Agardh (Chlorophyta). Planta 213:64-70.
29. Hanelt, D. & Nultsch, W. 1995. Field studies of photoinhibition show non-correlations between oxygen and fluorescence measurements in the Arctic red alga Palmaria palmata. J. Plant Physiol. 145:31-8.
30. Harvey, B. P., Gwynn-Jones, D. & Moore, P. J. 2013. Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecol. Evol. 3:1016-30.
31. Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S., Greenfield, P., Gomez, E., Harvell, C. D. et al. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318:1737-42.
32. Hughes, T. P., Graham, N. A. J., Jackson, J. B. C., Mumby, P. J. & Steneck, R. S. 2010. Rising to the challenge of sustaining coral reef resilience. Trends Ecol. Evol. 25:633-42.
33. Hughes, T. P., Rodrigues, M. J., Bellwood, D. R., Ceccarelli, D., Hoegh-Guldberg, O., McCook, L., Moltschaniwskyj, N., Pratchett, M. S., Steneck, R. S. & Willis, B. 2007. Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr. Biol. 17:360-5.
34. Humphrey, G. F. 1975. The photosynthesis: respiration ratio of some unicellular marine algae. J. Exp. Mar. Biol. Ecol. 18:111-9.
35. IPCC. 2007. The physical science basis. In Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K. B., Tignor, M. & Miller, H. L. [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. Summary for Policymakers. Cambridge University Press, Cambridge, UK, pp. 996.
36. 2 concentrations. Glob. Change Biol. 8:831-40.
37. Israel, A., Katz, S., Dubinsky, Z., Merrill, J. E. & Friedlander, M. 1999. Photosynthetic inorganic carbon utilization and growth of Porphyra linearis (Rhodophyta). J. Appl. Phycol. 11:447-53.
38. Jompa, J. & McCook, L. J. 2003. Coral-algal competition: macroalgae with different properties have different effects on corals. Mar. Ecol. Prog. Ser. 258:87-95.
39. Jones, R. S. 1968. Ecological relationships in Hawaiian and Johnston Island acanthurids (surgeonfishes). Micronesica 4:310-61.
40. 2 specificity of ribulose 1, 5-bisphosphate carboxylase/oxygenase. Planta 161:308-13.
41. Kleypas, J. A., McManus, J. W. & Meñez, L. A. B. 1999. Environmental limits to coral reef development: where do we draw the line? Am. Zool. 39:146-59.
42. 2 enrichment experiment on Heron Island (GBR). Sci. Rep. 2:1-9.
43. Koop, K., Booth, D., Broadbent, A., Brodie, J., Bucher, D., Capone, D., Coll, J. et al. 2001. ENCORE: the effect of nutrient enrichment on coral reefs. Synthesis of results and conclusions. Mar. Pollut. Bull. 42:91-120.
44. Lapointe, B. E. 1987. Phosphorus- and nitrogen-limited photosynthesis and growth of Gracilaria tikvahiae (Rhodophyceae) in the Florida Keys: an experimental field study. Mar. Biol. 93:561-8.
45. Larkum, A. W. D., Douglas, S. E. & Raven, J. A. 2004. Advances in photosynthesis and respiration, volume 14: 'photosynthesis in algae'. In Govindjee [Ed.] Photosynthesis Research. Springer, Dordrecht, The Netherlands, pp. 109-11. Available at: http://www.life.illinois.edu/govindjee/cv.html
46. Larkum, A. W. D. & Koop, K. 1997. ENCORE, Algal productivity and possible paradigm shifts. In Lessios, H. A. & Macintyre, I. G. [Eds.] 8th International Coral Reef Symposium. Smithsonian Tropical Research Institute, Panama, pp. 881-4.
47. Larned, S. T. 1998. Nitrogen- versus phosphorus-limited growth and sources of nutrients for coral reef macroalgae. Mar. Biol. 132:409-21.
48. Littler, M. M., Littler, D. S. & Titlyanov, E. A. 1991. Comparisons of N- and P-limited productivity between high granitic islands versus low carbonate atolls in the Seychelles Archipelago: a test of the relative-dominance paradigm. Coral Reefs 10:199-209.
49. Lobban, C. & Harrison, P. 1994. Seaweed Ecology and Physiology. Cambridge University Press, Cambridge, 366 pp.
50. Maberly, S. C. 1990. Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. J. Phycol. 26:439-49.
51. Mathieson, A. C. & Dawes, C. J. 1986. Photosynthetic responses of Florida seaweeds to light and temperature: a physiological survey. Bull. Mar. Sci. 38:512-24.
52. McCook, L. J., Jompa, J. & Diaz-Pulido, G. 2001. Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19:400-17.
53. Michel, G., Tonon, T., Scornet, D., Cock, J. M. & Kloareg, B. 2010. Central and storage carbon metabolism of the brown alga Ectocarpus siliculosus: insights into the origin and evolution of storage carbohydrates in Eukaryotes. New Phytol. 188:67-81.
54. Miller, M. W., Hay, M. E., Miller, S. L., Malone, D., Sotka, E. E. & Szmant, A. M. 1999. Effects of nutrients versus herbivores on reef algae: a new method for manipulating nutrients on coral reefs. Limnol. Oceanogr. 44:1847-61.
55. Müller, P., Li, X. P. & Niyogi, K. K. 2001. Non-photochemical quenching. A response to excess light energy. Plant Physiol. 125:1558-66.
56. Murchie, E. H. & Niyogi, K. K. 2011. Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol. 155:86-92.
57. Niyogi, K. K. 1999. Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:333-59.
58. Nyström, M., Folke, C. & Moberg, F. 2000. Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol. Evol. 15:413-7.
59. Nyström, M., Graham, N. A. J., Lokrantz, J. & Norström, A. V. 2008. Capturing the cornerstones of coral reef resilience: linking theory to practice. Coral Reefs 27:795-809.
60. Paerl, H. W. & Huisman, J. 2009. Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environ. Microbiol. Rep. 1:27-37.
61. Parsons, T. R., Maita, Y. & Lalli, C. M. 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, Oxford, New York, Sydney, 173 pp.
62. Phillips, J. C. & Hurd, C. L. 2004. Kinetics of nitrate, ammonium, and urea uptake by four intertidal seaweeds from New Zealand. J. Phycol. 40:534-45.
63. Raven, J. A. 1997. Putting the C in phycology. Eur. J. Phycol. 32:319-33.
64. Raven, J. A. & Hurd, C. L. 2012. Ecophysiology of photosynthesis in macroalgae. Photosynth. Res. 113:105-25.
65. Reef, R., Pandolfi, J. M. & Lovelock, C. E. 2012. The effect of nutrient enrichment on the growth, nucleic acid concentrations, and elemental stoichiometry of coral reef macroalgae. Ecol. Evol. 2:1985-95.
66. Rogelj, J., Meinshausen, M. & Knutti, R. 2012. Global warming under old an new scenarios using IPCC climate sensitivity range estimates. Nature Clim. Change 2:248-53.
67. Rogers, R. W. 1997. Brown algae on heron reef flat, Great Barrier Reef, Australia: spatial, seasonal and secular variation in cover. Bot. Mar. 40:113-7.
68. Schaffelke, B. 1999. Short-term nutrient pulses as tools to assess responses of coral reef macroalgae to enhanced nutrient availability. Mar. Ecol. Prog. Ser. 182:305-10.
69. Schaffelke, B. & Klumpp, D. W. 1998a. Nutrient-limited growth of the coral reef macroalga Sargassum baccularia and experimental growth enhancement by nutrient addition in continuous flow culture. Mar. Ecol. Prog. Ser. 164:199-211.
70. Schaffelke, B. & Klumpp, D. W. 1998b. Short-term nutrient pulses enhance growth and photosynthesis of the coral reef macroalga Sargassum baccularia. Mar. Ecol. Prog. Ser. 170:95-105.
71. Smith, J. E., Shaw, M., Edwards, R. A., Obura, D., Pantos, O., Sala, E., Sandin, S. A., Smriga, S., Hatay, M. & Rohwer, F. L. 2006. Indirect effects of algae on coral: algal-mediated, microbe induced coral mortality. Ecol. Lett. 9:835-45.
72. Smith, J. S., Smith, C. S. & Hunter, C. H. 2001. An experimental analysis of the effects of herbivory and nutrient enrichment on benthic community dynamics on a Hawaiian reef. Coral Reefs 19:332-42.
73. Surif, M. B. & Raven, J. A. 1989. Exogenous inorganic carbon-sources for photosynthesis in seawater by members of the Fucales and the Laminariales (Phaeophyta) - ecological and taxonomic implications. Oecologia 78:97-105.
74. Wheeler, P. A. & North, W. J. 1980. Effect of nitrogen supply on nitrogen content and growth rate of juvenile Macrocystis pyrifera (Phaeophyta) sporophytes. J. Phycol. 16:577-82.
75. Wild, C., Haas, A., Naumann, M. S., Mayr, C. & el-Zibdah, M. 2008. Comparative Investigation of Organic Matter Release by Corals and Benthic Reef Algae - Implications for Pelagic and Benthic Microbial Metabolism. 11th International Coral Reef Symposium, Ft. Lauderdale, FL, pp 1319-23.
76. Wisshak, M., Schönberg, C. H. L., Form, A. & Freiwald, A. 2012. Ocean Acidification Accelerates Reef Bioerosion. PLoS ONE 7:e45124.
77. 2-induced ocean acidification mediates the physiological performance of a green tide alga. Plant Physiol. 160:1762-9.
78. Zapata, M., Rodriguez, F. & Garrido, J. L. 2000. Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C-8 column and pyridine-containing mobile phases. Mar. Ecol. Prog. Ser. 195:29-45.
79. 2 in Seawater: Equilibrium, Kinetics, Isotopes. Elsevier Science, Amsterdam, 346 pp.