The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1627, 2013, Pages

  Connell, Sean D ^a   Kroeker, Kristy J ^b   Fabricius, Katharina E ^c   Kline, David I ^d   Russell, Bayden D ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF CALIFORNIA DAVIS   (United States)

^c AUSTRALIAN INSTITUTE OF MARINE SCIENCE   (Australia)

^d INTEGRATIVE OCEANOGRAPHY DIVISION   (United States)

Author keywords

Carbon dioxide; Competition; Coral reef; Kelp; Multiple stressor; Phase shift

Indexed keywords

ACIDIFICATION; CARBON DIOXIDE; CORAL REEF; DATA SET; DOMINANCE; ECOSYSTEM; OCEAN; RESILIENCE;

CARBON DIOXIDE; SEA WATER;

BIOFILM; BIOLOGICAL MODEL; CHEMISTRY; CORAL REEF; GROWTH, DEVELOPMENT AND AGING; MACROCYSTIS; METABOLISM; PH; SEA; SPECIES DIFFERENCE; COMPETITION; KELP; MULTIPLE STRESSOR; PHASE-SHIFT; REVIEW;

BIOFILMS; CARBON DIOXIDE; CORAL REEFS; HYDROGEN-ION CONCENTRATION; MACROCYSTIS; MODELS, BIOLOGICAL; OCEANS AND SEAS; SEAWATER; SPECIES SPECIFICITY;

CARBON DIOXIDE; COMPETITION; CORAL REEF; KELP; MULTIPLE STRESSOR; PHASE-SHIFT;

EID: 84883046436     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0442     Document Type: Review

References (90)

1. Wootton JT. 1994 The nature and consequences of indirect effects in ecological communities. Annu. Rev. Ecol. Syst. 25, 443-466. (doi:10.1146/annurev. es.25.110194.002303)
2. Suding KN, Hobbs RJ. 2009 Threshold models in restoration and conservation: a developing framework. Trends Ecol. Evol. 24, 271-279. (doi:10. 1016/j.tree.2008.11.012)
3. Jackson BC. 2001 What was natural in the coastal oceans? Proc. Natl Acad. Sci. USA 98, 5411-5418. (doi:10.1073/pnas.091092898)
4. Crain CM, Kroeker K, Halpern BS. 2008 Interactive and cumulative effects of multiple human stressors in marine systems. Ecol. Lett. 11, 1304-1315. (doi:10.1111/j.1461-0248.2008.01253.x)
5. Scheffer M, Carpenter SR. 2003 Catastrophic regime shifts in ecosystems: linking theory to observation. Trends Ecol. Evol. 18, 648-656. (doi:10.1016/j.tree. 2003.09.002)
6. Hughes TP et al. 2007 Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr. Biol. 17, 360-365. (doi:10.1016/j.cub.2006. 12.049)
7. Lebel L, Anderies JM, Campbell B, Folke C, Hatfield-Dodds S, Hughes TP, Wilson J. 2006 Governance and the capacity to manage resilience in regional socialecological systems. Ecol. Soc. 11, 19.
8. Godbold JA, Solan M. 2013 Long-term effects of warming and ocean acidification are modified by seasonal variation in species responses and environmental conditions. Phil. Trans. R. Soc. B. 368, 20130186. (doi:10.1098/rstb.2013.0186)
9. Russell BD, Harley CDG, Wernberg T, Mieszkowska N, Widdicombe S, Hall-Spencer JM, Connell SD. 2012 Predicting ecosystem shifts requires new approaches that integrate the effects of climate change across entire systems. Biol. Lett. 8, 164-166. (doi:10.1098/rsbl.2011.0779)
10. 2 problem. Annu. Rev. Mar. Sci. 1, 169-192. (doi:10.1146/annurev. marine.010908.163834)
11. Hoegh-Guldberg O et al. 2007 Coral reefs under rapid climate change and ocean acidification. Science 318, 1737-1742. (doi:10.1126/science. 1152509)
12. Kroeker KJ, Kordas RL, Crim RN, Singh GG. 2010 Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett. 13, 1419-1434. (doi:10.1111/j.1461-0248.2010. 01518.x)
13. 2-induced ocean acidification. Geology 37, 1131-1134. (doi:10.1130/g30210a.1)
14. 2 on calcium carbonate structures in different marine organisms. Mar. Biol. Res. 7, 565-575. (doi:10.1080/17451000.2010.547200)
15. Byrne M. 2011 Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Oceanogr. Mar. Biol., An Annu. Rev. 49, 1-42.
16. Wootton JT, Pfister CA, Forester JD. 2008 Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. Proc. Natl Acad. Sci. USA 105, 18 848-18 853. (doi:10. 1073/pnas.0810079105)
17. Orr JC et al. 2005 Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681-686. (doi:10.1038/nature04095)
18. 2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proc. R. Soc. B 277, 1409-1415. (doi:10.1098/rspb.2009.2069)
19. Harley CDG, Anderson KM, Demes KW, Jorve JP, Kordas RL, Coyle TA, Graham MH. 2012 Effects of climate change on global seaweed communities. J. Phycol. 48, 1064-1078. (doi:10.1111/j.1529-8817.2012.01224.x)
20. Koch M, Bowes G, Ross C, Zhang XH. 2013 Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob. Change Biol. 19, 103-132. (doi:10.1111/j.1365-2486.2012.02791.x)
21. Harpole WS et al. 2011 Nutrient co-limitation of primary producer communities. Ecol. Lett. 14, 852-862. (doi:10.1111/j.1461-0248.2011.01651.x)
22. 2 concentrating mechanisms, and their regulation. Funct. Plant Biol. 29, 335-347. (doi:10.1071/pp01195)
23. 2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu. Rev. Plant Biol, 56, 99-131. (doi:10.1146/annurev. arplant.56.032604.144052)
24. Hurd CL, Hepburn CD, Currie KI, Raven JA, Hunter KA. 2009 Testing the effects of ocean acidification on algal metabolism: considerations for experimental design. J. Phycol. 45, 1236-1251. (doi:10.1111/j.1529-8817.2009.00768.x)
25. 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. (doi:10.1111/j.1529-8817. 2011.01085.x)
26. 2 on a marine habitat. J. Appl. Ecol. 50, 51-58. (doi:10.1111/1365-2664.12019)
27. Rost B, Riebesell U, Burkhardt S, Sultemeyer D. 2003 Carbon acquisition of bloom-forming marine phytoplankton. Limnol. Oceanogr. 48, 55-67. (doi:10.4319/lo.2003.48.1.0055)
28. Beardall J, Raven JA. 2004 The potential effects of global climate change on microalgal photosynthesis, growth and ecology. Phycologia 43, 26-40. (doi:10.2216/i0031-8884-43-1-26.1)
29. 2 ocean. Glob. Change Biol. 17, 2488-2497. (doi:10.1111/j.1365-2486.2011. 02411.x)
30. 2 enhances the competitive strength of seaweeds over corals. Ecol. Lett. 14, 156-162. (doi:10.1111/j.1461-0248.2010. 01565.x)
31. 2 and nutrient regimes. Oecologia 172, 575-583. (doi:10.1007/s00442-012-2507-5)
32. Connell SD, Russell BD, Turner DJ, Shepherd SA, Kildea T, Miller DJ, Airoldi L, Cheshire A. 2008 Recovering a lost baseline: missing kelp forests from a metropolitan coast. Mar. Ecol. Prog. Ser. 360, 63-72. (doi:10.3354/meps07526)
33. Gorman D, Russell BD, Connell SD. 2009 Land-tosea connectivity: linking human-derived terrestrial subsidies to subtidal habitat change on open rocky coasts. Ecol. Appl. 19, 1114-1126. (doi:10.1890/ 08-0831.1)
34. Allgeier JE, Rosemond AD, Layman CA. 2011 The frequency and magnitude of non-additive responses to multiple nutrient enrichment. J. Appl. Ecol. 48, 96-101. (doi:10.1111/j.1365-2664.2010.01894.x)
35. Schiel DR, Foster MS. 1986 The structure of subtidal algal stands in temperate waters. Oceanogr. Mar. Biol., An Annu. Rev. 24, 265-307.
36. Chapin FS, Bloom AJ, Field CB, Waring RH. 1987 Plant-responses to multiple environmental factors. Bioscience 37, 49-57. (doi:10.2307/1310177)
37. Venterink HO, Wassen MJ, Verkroost AWM, de Ruiter PC. 2003 Species richness-productivity patterns differ between N-, P-, and K-limited wetlands. Ecology 84, 2191-2199. (doi:10.1890/01-0639)
38. Tilman D, Lehman C. 2001 Human-caused environmental change: impacts on plant diversity and evolution. Proc. Natl Acad. Sci. USA 98, 5433-5440. (doi:10.1073/pnas.091093198)
39. Katsikatsou M, Anestis A, Portner HO, Vratsistas A, Aligizaki K, Michaelidis B. 2012 Field studies and projections of climate change effects on the bearded horse mussel Modiolus barbatus in the Gulf of Thermaikos, Greece. Mar. Ecol. Prog. Ser. 449, 183-196. (doi:10.3354/meps09550)
40. Connell SD, Russell BD, Irving AD. 2011 Can strong consumer and producer effects be reconciled to better forecast 'catastrophic' phase-shifts in marine ecosystems?. J. Exp. Mar. Biol. Ecol. 400, 296-301. (doi:10.1016/j.jembe.2011.02.031)
41. Hughes TP. 1994 Catastrophes, phase-shifts, and large-scale degradation of a Caribbean coral-reef. Science 265, 1547-1551. (doi:10.1126/science.265. 5178.1547)
42. Jackson JBC et al. 2001 Historical overfishing and the recent collapse of coastal ecosystems. Science 293, 629-638. (doi:10.1126/science.1059199)
43. Sanford E. 1999 Regulation of keystone predation by small changes in ocean temperature. Science 283, 2095-2097. (doi:10.1126/science.283.5410.2095)
44. Suttle KB, Thomsen MA, Power ME. 2007 Species interactions reverse grassland responses to changing climate. Science 315, 640-642. (doi:10.1126/ science.1136401)
45. Kawai T, Tokeshi M. 2007 Testing the facilitationcompetition paradigm under the stress-gradient hypothesis: decoupling multiple stress factors. Proc. R. Soc. B 274, 2503-2508. (doi:10.1098/rspb. 2007.0871)
46. Caldeira K, Wickett ME. 2003 Anthropogenic carbon and ocean pH. Nature 425, 365. (doi:10.1038/ 425365a)
47. Kroeker KJ, Micheli F, Gambi MC. 2012 Ocean acidification causes ecosystem shifts via altered competitive interactions. Nat. Clim. Change 3, 156-159. (doi:10.1038/nclimate1680)
48. Fabricius KE et al. 2011 Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat. Clim. Change 1, 165-169. (doi:10.1038/nclimate1122)
49. Krebs CJ. 2009 Ecology: the experimental analysis of distribution and abundance, 6th edn. 688 p. San Francisco, CA: Benjamin Cummings.
50. Bruno JF, Sweatman H, Precht WF, Selig ER, Schutte VGW. 2009 Assessing evidence of phase shifts from coral to macroalgal dominance on coral reefs. Ecology 90, 1478-1484. (doi:10.1890/ 08-1781.1)
51. Foster MS, Schiel DR. 2010 Loss of predators and the collapse of southern California kelp forests (?): alternatives, explanations and generalizations. J. Exp. Mar. Biol. Ecol. 393, 59-70. (doi:10.1016/j. jembe.2010.07.002)
52. Connell SD, Irving AD. 2009 The subtidal ecology of rocky coasts: local-regional-biogeographic patterns and their experimental analysis. In Marine macroecology (eds JD Witman, R Kaustuv), pp. 392-417. Chicago, IL: University of Chicago Press.
53. Levin SA. 1992 The problem of pattern and scale in ecology. Ecology 73, 1943-1967. (doi:10.2307/ 1941447)
54. Pedersen MF, Borum J. 1996 Nutrient control of algal growth in estuarine waters. Nutrient limitation and the importance of nitrogen requirements and nitrogen storage among phytoplankton and species of macroalgae. Mar. Ecol. Prog. Ser. 142, 261-272. (doi:10.3354/meps142261)
55. Connell SD, Foster MS, Airoldi L. In press. What are algal turfs? Towards a better description of turfs. Mar. Ecol. Prog. Ser.
56. Bellwood DR, Hughes TP, Folke C, Nystrom M. 2004 Confronting the coral reef crisis. Nature 429, 827-833. (doi:10.1038/nature02691)
57. Martinez JA, Smith CM, Richmond RH. 2012 Invasive algal mats degrade coral reef physical habitat quality. Estuar. Coast Shelf Sci. 99, 42-49. (doi:10.1016/j.ecss.2011.12.022)
58. Hauri C, Fabricius KE, Schaffelke B, Humphrey C. 2010 Chemical and physical environmental conditions underneath mat-and canopy-forming macroalgae, and their effects on understorey corals. PLoS ONE 5, e12685. (doi:10.1371/journal.pone. 0012685)
59. Jompa J, McCook LJ. 2002 Effects of competition and herbivory on interactions between a hard coral and a brown alga. J. Exp. Mar. Biol. Ecol. 271, 25-39. (doi:10.1016/s0022-0981(02)00040-0)
60. Vermeij MJA, Sandin SA. 2008 Density-dependent settlement and mortality structure the earliest life phases of a coral population. Ecology 89, 1994-2004. (doi:10.1890/07-1296.1)
61. Gorman D, Connell SD. 2009 Recovering subtidal forests on human-dominated landscapes. J. Appl. Ecol. 46, 1258-1265. (doi:10.1111/j.1365-2664. 2009.01711.x)
62. Benedetti-Cecchi L, Pannacciulli F, Bulleri F, Moschella PS, Airoldi L, Relini G, Cinelli F. 2001 Predicting the consequences of anthropogenic disturbance: large-scale effects of loss of canopy algae on rocky shores. Mar. Ecol. Prog. Ser. 214, 137-150. (doi:10.3354/meps214137)
63. Eriksson BK, Johansson G, Snoeijs P. 2002 Longterm changes in the macroalgal vegetation of the inner Gullmar Fjord, Swedish Skagerrak coast. J. Phycol. 38, 284-296. (doi:10.1046/j.1529-8817. 2002.00170.x)
64. Airoldi L. 2003 The effects of sedimentation on rocky coast assemblages. Oceanogr. Mar. Biol., An Annu. Rev. 41, 161-236.
65. Vermeij MJA, van Moorselaar I, Engelhard S, Hornlein C, Vonk SM, Visser PM. 2010 The effects of nutrient enrichment and herbivore abundance on the ability of turf algae to overgrow coral in the Caribbean. PLoS ONE 5, e14312. (doi:10.1371/ journal.pone.0014312)
66. Hofmann GE et al. 2011 High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS ONE 6, e28983. (doi:10.1371/journal.pone.0028983)
67. Feely RA, Sabine CL, Hernandez-Ayon JM, Ianson D, Hales B. 2008 Evidence for upwelling of corrosive 'acidified' water onto the continental shelf. Science 320, 1490-1492. (doi:10.1126/science.1155676)
68. Cohen J. 1988 Statistical power analysis for the behavioural sciences, 2nd edn. Hillsdale, NJ: Lawrence Erlbaum Associates.
69. IPCC. 2007 Climate change 2007: the physical science basis. Contribution of Working Group 1 to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press.
70. 2 enrichment experiment on Heron Island (GBR). Sci. Rep. 2, 413. (doi:10.1038/srep00413)
71. 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. (doi:10.1038/nature07051).
72. 2 vents is dependent upon species acid-base and ion-regulatory abilities. Mar. Pollut. Bull. (doi:10.1016/j.marpolbul.2012.11.040)
73. 2 ocean. Proc. Natl Acad. Sci. (doi:10. 1073/pnas.1216464110)
74. Kroeker KJ, Micheli F, Gambi MC, Martz TR. 2011 Divergent ecosystem responses within a benthic marine community to ocean acidification. Proc. Natl Acad. Sci. USA 108, 14 515-14 520. (doi:10.1073/ pnas.1107789108)
75. Duarte CM, Hendriks IE, Moore TS, Olsen YS, Steckbauer A, Ramajo L, Carstensen J, Trotter JA, McCulloch M. 2013 Is ocean acidification an openocean syndrome? Understanding anthropogenic impacts on seawater pH. Estuar. Coasts 36, 221-236. (doi:10.1007/s12237-013-9594-3)
76. Vitousek P, Mooney H, Lubchenco J, Melillo J. 1997 Human domination of earth's ecosystems. Science 277, 494-499. (doi:10.1126/science.277. 5325.494)
77. 2 and nutrient driven change in subtidal rocky habitats. Glob. Change Biol. 15, 2153-2162. (doi:10.1111/j.1365-2486.2009.01886.x)
78. Bender D, Diaz-Pulido G, Dove S. 2012 Effects of macroalgae on corals recovering from disturbance. J. Exp. Mar. Biol. Ecol. 429, 15-19. (doi:10.1016/ j.jembe.2012.06.014).
79. Schneider K, Erez J. 2006 The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol. Oceanogr. 51, 1284-1293. (doi:10.4319/lo.2006.51. 3.1284)
80. Lubchenco J. 1978 Plant species diversity in a marine intertidal community: importance of herbivore food preference and algal competitive abilities. Am. Nat. 112, 23-39. (doi:10.1086/ 283250)
81. Carpenter RC. 1986 Parttitioning herbivory and its effects on coral-reef algal communities. Ecol. Monogr. 56, 345-363. (doi:10.2307/1942551).
82. Worm B, Lotze HK. 2006 Effects of eutrophication, grazing, and algal blooms on rocky shores. Limnol. Oceanogr. 51, 569-579. (doi:10.4319/lo.2006.51. 1_part_2.0569)
83. 2 may rival its direct effects. Mar. Ecol. Prog. Ser.
84. Rossoll D, Bermudez R, Hauss H, Schulz KG, Riebesell U, Sommer U, Winder M. 2012 Ocean acidification-induced food quality deterioration constrains trophic transfer. PLoS ONE 7, e34737. (doi:10.1371/journal.pone.0034737)
85. Arnold T, Mealey C, Leahey H, Miller AW, Hall-Spencer JM, Milazzo M, Maers K. 2012 Ocean acidification and the loss of phenolic substances in marine plants. PLoS ONE 7, e35107. (doi:10.1371/ journal.pone.0035107)
86. O'Connor MI. 2009 Warming strengthens an herbivore-plant interaction. Ecology 90, 388-398. (doi:10.1890/08-0034.1)
87. Russell BD, Connell SD, Findlay HS, Tait K, Widdicombe S, Mieszkowska N. 2013 Ocean acidification and rising temperatures may increase biofilm primary productivity but decrease grazer consumption. Phil. Trans. R. Soc. B 368, 20120438. (doi:10.1098/rstb.2012.0438)
88. 3 system in the oceans. Science 305, 362-366. (doi:10.1126/science.1097329)
89. Darling ES, Côté IM. 2008 Quantifying the evidence for ecological synergies. Ecol. Lett. 11, 1278-1286. (doi:10.1111/j.1461-0248.2008.01243.x)
90. Hughes TP, Linares C, Dakos V, van de Leemput IA, van Nes EH. 2013 Living dangerously on borrowed time during slow, unrecognized regime shifts. Trends Ecol. Evol. 28, 149-155. (doi:10.1016/j.tree. 2012.08.022)