Strategies of dissolved inorganic carbon use in macroalgae across a gradient of terrestrial influence: implications for the Great Barrier Reef in the context of ocean acidification

Coral Reefs

Volumn 35, Issue 4, 2016, Pages 1327-1341

  Diaz Pulido, Guillermo ^a,b   Cornwall, Christopher ^c,d,e   Gartrell, Patrick ^a   Hurd, Catriona ^e   Tran, Dien V ^a  

^a GRIFFITH UNIVERSITY   (Australia)

^b Australian Research Council Centre of Excellence for Coral Reef Studies   (Australia)

^c UNIVERSITY OF OTAGO   (New Zealand)

^d UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^e UNIVERSITY OF TASMANIA   (Australia)

Author keywords

Carbon concentrating mechanisms; Carbon dioxide; Great Barrier Reef; Ocean acidification; Seaweeds; Terrestrial runoff

Indexed keywords

ADAPTATION; CARBON DIOXIDE; CORAL REEF; DISSOLVED INORGANIC CARBON; LIGHT USE EFFICIENCY; MACROALGA; OCEAN ACIDIFICATION; RUNOFF; SEAWEED;

AUSTRALIA; CORAL SEA; GREAT BARRIER REEF; QUEENSLAND;

ALGAE; ANTHOZOA;

EID: 84978767521     PISSN: 07224028     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00338-016-1481-5     Document Type: Article

References (57)

1. Anthony KRN, Diaz-Pulido G, Verlinden N, Tilbrook B, Andersson AJ (2013) Benthic buffers and boosters of ocean acidification on coral reefs. Biogeosciences 10:4897–4909
2. 2 emission scenarios and nutrient enrichment on a common coral reef macroalga is modified by temporal effects. J Phycol 50:203–215
3. 13C values in marine organisms from the Great Barrier Reef. Aust J Plant Physiol 3:25–32
4. Brodie JE, Devlin M, Haynes D, Waterhouse J (2011) Assessment of the eutrophication status of the Great Barrier Reef Lagoon (Australia). Biogeochemistry 106:281–302
5. Bruno JF, Sweatman H, Precht WF, Selig ER, Schutte VG (2009) Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology 90:1478–1484
6. 2 as a resource among competitors for ecosystem dominance. Philos Trans R Soc Lond 368:20120442
7. 2 by macroalgae in a temperate subtidal ecosystem. Photosynth Res 124:181–190
8. 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
9. De’ath G, Fabricius KE (2010) Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef. Ecol Appl 20:840–850
10. Diaz-Pulido G, Harii S, McCook LJ, Hoegh-Guldberg O (2010) The impact of benthic algae on the settlement of a reef-building coral. Coral Reefs 29:203–208
11. 2 enhances the competitive strength of seaweeds over corals. Ecol Lett 14:156–162
12. Diaz-Pulido G, Anthony KRN, Kline DI, Dove S, Hoegh-Guldberg O (2012) Interactions between ocean acidification and warming on the mortality and dissolution of coralline algae. J Phycol 48:32–39
13. 2 measurements. North Pacific Marine Science Organization (PICES Special Publication, 3), Sidney, British Columbia
14. Duarte CM, Hendriks IE, Moore TS, Olsen YS, Steckbauer A, Ramajo L, Carstensen J, Trotter JA, McCulloch M (2013) Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on seawater pH. Estuar Coast 36:221–236
15. Enochs IC, Manzello DP, Donham EM, Kolodziej G, Okano R, Johnston L, Young C, Iguel J, Edwards CB, Fox MD, Valentino L, Johnson S, Benavente D, Clark SJ, Carlton R, Burton T, Eynaud Y, Price NN (2015) Shift from coral to macroalgae dominance on a volcanically acidified reef. Nature Clim Chang 5:1083–1088
16. Fabricius KE, De’ath G, McCook LJ, Turak E, Williams DM (2005) Changes in algal, coral and fish assemblages along water quality gradients on the inshore Great Barrier Reef. Mar Pollut Bull 51:384–398
17. Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner NGMS, Lough JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nature Clim Chang 1:165–169
18. Fabricius KE, Cooper TF, Humphrey C, Uthicke S, De’ath G, Davidson J, Legrand H, Thompson A, Schaffelke B (2012) A bioindicator system for water quality on inshore coral reefs of the Great Barrier Reef. Mar Pollut Bull 65:320–332
19. Fernandez PA, Hurd CL, Roleda MY (2014) Bicarbonate uptake via the anion exchange protein is the main mechanism of inorganic carbon acquisition by the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae) under variable pH. J Phycol 50:998–1008
20. 12C comparison of food webs in Caribbean seagrass meadows and coral reefs. Aquat Bot 14:389–398
21. 2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131
22. Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia MC (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99
23. Hay ME (1981) Herbivory, algal distribution, and the maintenance of between-habitat diversity on a tropical fringing reef. Am Nat 118:520–540
24. 2 ocean. Glob Change Biol 17:2488–2497
25. 2-concentrating mechanism of diatoms. Proc Natl Acad Sci USA 108:3830–3837
26. Hughes TP (1994) Catastrophes, phase-shifts and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551
27. Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642
28. Hurd CL, Harrison PJ, Bischof K, Lobban CS (2014) Seaweed ecology and physiology. Cambridge University Press, Cambridge
29. Hurd CL, Hepburn CD, Currie KI, Raven JA, Hunter KA (2009) Testing the effects of ocean acidification on algal metabolism: Considerations for experimental designs. J Phycol 45:1236–1251
30. Johnson MD, Price NN, Smith JE (2014) Contrasting effects of ocean acidification on tropical fleshy and calcareous algae. PeerJ 2:e411
31. Koch M, Bowes G, Ross C, Zhang XH (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Chang Biol 19:103–132
32. 2 and warming. ICES J Mar Sci 73:693–703
33. Kübler JE, Dudgeon SR (2015) Predicting effects of ocean acidification and warming on algae lacking carbon concentrating mechanisms. PLoS One 10:e0132806
34. 2 on the seaweed Lomentaria articulata. Plant Cell Environ 22:1303–1310
35. 2 system calculations. ORNL/CDIAC-105, Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, Tennessee
36. Linares C, Vidal M, Canals M, Kersting DK, Amblas D, Aspillaga E, Cebriįn E, Delgado-Huertas A, Dķaz D, Garrabou J, Hereu B, Navarro L, Teixidó N, Ballesteros E (2015) Persistent natural acidification drives major distribution shifts in marine benthic ecosystems. Proc R Soc B 282:20150587
37. 13C by marine plants. Oecologia 91:481–492
38. Marconi M, Giordano M, Raven JA (2011) Impact of taxonomy, geography, and depth on delta C-13 and delta N-15 variation in a large collection of macroalgae. J Phycol 47:1023–1035
39. McCook LJ (1996) Effects of herbivores and water quality on Sargassum distribution on the central Great Barrier Reef: cross-shelf transplants. Mar Ecol Prog Ser 139:179–192
40. McCook LJ (1999) Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18:357–367
41. McCook LJ, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19:400–417
42. Mumby PJ, Steneck RS (2008) Coral reef management and conservation in light of rapidly evolving ecological paradigms. Trends Ecol Evol 23:555–563
43. Murru M, Sandgren CD (2004) Habitat matters for inorganic carbon acquisition in 38 species of red macroalgae (Rhodophyta) from Puget Sound, Washington, USA. J Phycol 40:837–845
44. Nugues MM, Smith GW, Hooidonk RJ, Seabra MI, Bak RPM (2004) Algal contact as a trigger for coral disease. Ecol Lett 7:919–923
45. Olischlager M, Wiencke C (2013) Ocean acidification alleviates low-temperature effects on growth and photosynthesis of the red alga Neosiphonia harveyi (Rhodophyta). J Exp Bot 64:5587–5597
46. 2 concentrating mechanisms and environmental change. Aquat Bot 118:24–37
47. Raven JA, Giordano M, Beardall J, Maberly SC (2011) Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change. Photosynth Res 109:281–296
48. Raven JA, Ball LA, Beardall J, Giordano M, Maberly SC (2005) Algae lacking carbon-concentrating mechanisms. Can J Bot 83:879–890
49. Raven JA, Johnston AM, Kübler JE, Korb R, Mcinroy SG, Handley LL, Scrimgeour CM, Walker DI, Beardall J, Vanderklift M, Fredriksen S, Dunton KH (2002) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29:355–378
50. Schaffelke B, Mellors J, Duke NC (2005) Water quality in the Great Barrier Reef region: responses of mangrove, seagrass and macroalgal communities. Mar Pollut Bull 51:279–296
51. Smith JE, Price NN, Nelson CE, Haas AF (2013) Coupled changes in oxygen concentration and pH caused by metabolism of benthic coral reef organisms. Mar Biol 160:2437–2447
52. Smith JE, Shaw M, Edwards RA, Obura D, Pantos O, Sala E, Sandin SA, Smriga S, Hatay M, Rohwer FL (2006) Indirect effects of algae on coral: algae-mediated, microbe induced coral mortality. Ecol Lett 9:835–845
53. Steneck RS, Dethier MN (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69:476–498
54. Stepien CC (2015) Impacts of geography, taxonomy and functional group on inorganic carbon use patterns in marine macrophytes. J Ecol 103:1372–1383
55. Uthicke S, Furnas MJ, Lųnborg C (2014) Coral reefs on the edge? Carbon chemistry on inshore reefs of the Great Barrier Reef. PLoS One 9:e109092
56. Wismer S, Hoey AS, Bellwood DR (2009) Cross-shelf benthic community structure on the Great Barrier Reef: relationships between macroalgal cover and herbivore biomass. Mar Ecol Prog Ser 376:45–54
57. Zou D, Gao K, Luo H (2011) Short- and long-term effects of elevated CO2 on photosynthesis and respiration in the marine macroalga Hizikia fusiformis (Sargassaceae, Phaeophyta) grown at low and high N supplies. J Phycol 47:87–97