Global Warming and Ocean Acidification: Effects on Australian Seagrass Ecosystems

  • Ylva S. OlsenEmail author
  • Catherine Collier
  • Yan X. Ow
  • Gary A. Kendrick


As concentrations of atmospheric CO2 increase, mean temperatures across the globe rise, the carbon system equilibrium in the ocean shifts, and pH is reduced in a process termed Ocean Acidification (OA). These changes can dramatically alter seagrass meadows as both temperature and pH fundamentally influence biochemistry and physiology of plants. Seagrass responses to climate change are species-specific and dependent on interactions with other factors such as light intensity, nutrient availability and competition. The majority of seagrasses appear limited by the availability of dissolved inorganic carbon at current ocean pH, suggesting that rates of photosynthesis and growth are likely to increase with OA. Short- and intermediate term laboratory experiments have shown an increase in photosynthetic rates to increased pCO2. Longer-term studies (>1 year) indicate enhanced shoot proliferation resulting in meadows with high shoot density. Studies utilizing natural gradients in pCO2 that exist near shallow volcanic CO2 vents have shown that, overall, seagrasses appear to benefit from OA. Seagrasses photosynthesize across a range in temperatures, but rapidly decline above thermal optima. Respiration rates increase with warming at a faster rate than photosynthesis and reduces the overall photosynthesis-to-respiration ratio, and thus growth. While seagrasses can recover from moderate temperature stress, extreme temperatures result in mortality. Future changes in seagrass species distributions are predicted as sensitive species shift poleward. Foundation species, like seagrasses, have a large influence on their environment and their loss can significantly impact the functioning of the whole ecosystem. Despite a recent increase in climate-change research, we lack an understanding of how seagrass meadows are going to respond to the combined pressures of warming and OA. It is particularly difficult to predict longer-term responses and possible adaptation, and efforts should be focused in this area to determine how we can manage seagrasses to maximize resilience to climate change.


  1. Adams MP, Collier CJ, Uthicke S, Ow YX, Langlois L, O’Brien KR (2017) Model fit versus biological relevance: evaluating photosynthesis-temperature models for three tropical seagrass species. Sci Rep 7:39930Google Scholar
  2. Agawin NSR, Duarte CM, Fortes MD (1996) Nutrient limitation of Philippine seagrasses (Cape Bolinao, NW Philippines): in situ experimental evidence. Mar Ecol Prog Ser 138:233–243CrossRefGoogle Scholar
  3. Alcoverro T, Duarte CM, Romero J (1995) Annual growth dynamics of Posidonia oceanica: contribution of large-scale versus local factors to seasonality. Mar Ecol Prog Ser 120:203–210CrossRefGoogle Scholar
  4. Alexandre A, Silva J, Buapet P, Bjork M, Santos R (2012) Effects of CO2 enrichment on photosynthesis, growth, and nitrogen metabolism of the seagrass Zostera noltii. Ecol Evol 2(10):2620–2630. Scholar
  5. Apostolaki ET, Vizzini S, Hendriks IE, Olsen YS (2014) Seagrass ecosystem response to long-term high CO2 in a Mediterranean volcanic vent. Mar Environ Res 99:9–15. Scholar
  6. 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(4):e35107. Scholar
  7. Atkin OK, Bruhn D, Hurry VM, Tjoelker MG (2005) Evans review No. 2: the hot and the cold: unravelling the variable response of plant respiration to temperature. Funct Plant Biol 32(2):87–105. Scholar
  8. Beer S (1989) Photosynthesis and photorespiration of marine angiosperms. Aquat Bot 34:153–166CrossRefGoogle Scholar
  9. Beer S (1994) Mechanisms of inorganic carbon acquisition in marine macroalgae (with special reference to the Chlorophyta). Prog Phycol Res 10:179–207Google Scholar
  10. Beer S, Koch E (1996) Photosynthesis of marine macroalgae and seagrasses in globally changing CO2 environments. Mar Ecol Prog Ser 141:199–204CrossRefGoogle Scholar
  11. Beer S, Rehnberg J (1997) The acquisition of inorganic carbon by the seagrass Zostera marina. Aquat Bot 56(3–4):277–283. Scholar
  12. Beer S, Bjork M, Hellblom F, Axelsson L (2002) Inorganic carbon utilization in marine angiosperms (seagrasses). Funct Plant Biol 29(2–3):349–354. Scholar
  13. Beer S, Mtolera M, Lyimo T, Bjork M (2006) The photosynthetic performance of the tropical seagrass Halophila ovalis in the upper intertidal. Aquat Bot 84(4):367–371. Scholar
  14. Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273CrossRefPubMedPubMedCentralGoogle Scholar
  15. Björk M, Axelsson L, Beer S (2004) Why is Ulva intestinalis the only macroalga inhabiting isolated rockpools along the Swedish Atlantic coast? Mar Ecol Prog Ser 284:109–116CrossRefGoogle Scholar
  16. Boden TA, Marland G, Andres RJ (2015) Global, regional, and national fossil-fuel CO2 emissions. Carbon dioxide information analysis center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, Tenn., U.S.A.
  17. Borum J, Pederson O, Greve TM, Frannkovich TA, Zieman JC, Fourqurean JW, Madden CJ (2005) The potential role of plant oxygen and sulphide dynamics in die-off events of the tropical seagrass, Thalassia testudinum. J Ecol 93:148–158CrossRefGoogle Scholar
  18. Borum J, Pedersen O, Kotula L, Fraser MW, Statton J, Colmer TD, Kendrick GA (2016) Photosynthetic response to globally increasing CO2 of co-occurring temperate seagrass species. Plant Cell Environ 39(6):1240–1250. Scholar
  19. Bulthuis DA (1983) Effects of temperature on the photosynthesis-irradiance curve of the Australian seagrass, Heterozostera tasmanica. Mar Biol Lett 4:47–57Google Scholar
  20. Bulthuis DA (1987) Effects of temperature on photosynthesis and growth of seagrasses. Aquat Bot 27:27–40Google Scholar
  21. Burdige DJ, Zimmerman RC (2002) Impact of sea grass density on carbonate dissolution in Bahamian sediments. Limnol Oceanogr 47:1751–1763CrossRefGoogle Scholar
  22. Burdige DJ, Zimmerman RC, Hu X (2008) Rates of carbonate dissolution in permeable sediments estimated from pore-water profiles: the role of sea grasses. Limnol Oceanogr 53:549–565CrossRefGoogle Scholar
  23. Burkholder JM, Tomasko DA, Touchette BW (2007) Seagrasses and eutrophication. J Exp Mar Biol Ecol 350(1–2):46–72. Scholar
  24. Burnell OW, Connell SD, Irving AD, Watling JR, Russell BD (2014a) Contemporary reliance on bicarbonate acquisition predicts increased growth of seagrass Amphibolis antarctica in a high-CO2 world. Conserv Physiol 2(1).
  25. Burnell OW, Russell BD, Irving AD, Connell SD (2014b) Seagrass response to CO2 contingent on epiphytic algae: indirect effects can overwhelm direct effects. Oecologia 176:871–882. Scholar
  26. Cambridge ML, Hocking PJ (1997) Annual primary production and nutrient dynamics of the seagrasses Posidonia sinuosa and Posidonia australis in south-western Australia. Aquat Bot 59:277–295CrossRefGoogle Scholar
  27. Campbell JE, Fourqurean JW (2013a) Effects of in situ CO2 enrichment on the structural and chemical characteristics of the seagrass Thalassia testudinum. Mar Biol 160(6):1465–1475. Scholar
  28. Campbell JE, Fourqurean JW (2013b) Mechanisms of bicarbonate use influence the photosynthetic carbon dioxide sensitivity of tropical seagrasses. Limnol Oceanogr 58(3):839–848. Scholar
  29. Campbell JE, Fourqurean JW (2014) Ocean acidification outweighs nutrient effects in structuring seagrass epiphyte communities. J Ecol 102(3):730–737. Scholar
  30. Campbell SJ, McKenzie LJ, Kerville SP (2006) Photosynthetic responses of seven tropical seagrasses to elevated seawater temperature. J Exp Mar Biol Ecol 330(2):455–468CrossRefGoogle Scholar
  31. Collier CJ, Waycott M (2014) Temperature extremes reduce seagrass growth and induce mortality. Mar Pollut Bull 83(2):483–490.
  32. Collier CJ, Lavery PS, Masini RJ, Ralph PJ (2007) Morphological, growth and meadow characteristics of the seagrass Posidonia sinuosa along a depth-related gradient of light availability. Mar Ecol Prog Ser 337:103–115CrossRefGoogle Scholar
  33. Collier CJ, Uthicke S, Waycott M (2011) Thermal tolerance of two seagrass species at contrasting light levels: Implications for future distribution in the Great Barrier Reef. Limnol Oceanogr 56(6):2200–2210. Scholar
  34. Collier CJ, Adams M, Langlois L, Waycott M, O’Brien K, Maxwell P, McKenzie L (2016) Thresholds for morphological response to light reduction for four tropical seagrass species. Ecol Ind 67:358–366. Scholar
  35. Collier CJ, Ow YX, Langlois L, Uthicke S, Johansson CL, O’Brien KR, Hrebien V, Adams MP (2017) Optimum temperatures for net primary productivity of three tropical seagrass species. Front Plant Sci 23(8):1446.
  36. Collier CJ, Langlois L, Ow YX, Johansson C, Giammusso M, Adams MA, O’Brien K, Uthicke S (in prep) Photoacclimation and productivity responses to climate change in three seagrass speciesGoogle Scholar
  37. Darling ES, Côté IM (2008) Quantifying the evidence for ecological synergies. Ecol Lett 11:1278–1286CrossRefPubMedGoogle Scholar
  38. Delille D, Marty G, CansemiSoullard M, Frankignoulle M (1997) Influence of subantarctic Macrocystis bed metabolism in diel changes of marine bacterioplankton and CO2 fluxes. J Plankton Res 19(9):1251–1264. Scholar
  39. Demmig-Adams B (2003) Linking the xanthophyll cycle with thermal energy dissipation. Photosynth Res 76:73–80CrossRefPubMedGoogle Scholar
  40. Dennison WC (1987) Effects of light on seagrass photosynthesis, growth and depth distribution. Aquat Bot 27:15–26Google Scholar
  41. Devlin M, Wenger A, Waterhouse J, Alvarez-Romero J, Abbott B, da Silva ET (2011) Reef Rescue Marine Monitoring Program: flood plume monitoring annual report 2010–11. Incorporating results from the Extreme Weather Response Program flood plume monitoring. Australian Centre for Tropical Freshwater Research, Townsville, AustraliaGoogle Scholar
  42. Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929CrossRefPubMedGoogle Scholar
  43. Diaz-Almela E, Marbà N, Duarte CM (2007) Consequences of Mediterranean warming events in seagrass (Posidonia oceanica) flowering records. Glob Change Biol 13(1):224–235. Scholar
  44. Domingues CM, Church JA, White NJ, Gleckler PJ, Wijffels SE, Barker PM, Dunn JR (2008) Improved estimates of upper-ocean warming and multi-decadal sea-level rise. Nature 453(7198):1090–1096. Scholar
  45. Doney SC, Schimel DS (2007) Carbon and climate system coupling on timescales from the Precambrian to the anthropocene. Annu Rev Environ Resour 32:31–66. Scholar
  46. Doney SC, Ruckelshaus M, Emmett Duffy J, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N, Polovina J, Rabalais NN, Sydeman WJ, Talley LD (2012) Climate change impacts on marine ecosystems. Annu Rev Mar Sci 4(1):11–37. Scholar
  47. Drake LA, Dobbs FC, Zimmerman RC (2003) Effects of epiphyte load on optical properties and photosynthetic potential of the seagrasses Thalassia testudinum Banks ex Konig and Zostera marina L. Limnol Oceanogr 48(1):456–463CrossRefGoogle Scholar
  48. 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. Estuaries Coasts 36(2):221–236. Scholar
  49. Durako MJ (1993) Photosynthetic utilization of CO2(aq) and HCO3 in Thalassia testudinum (Hydrocharitaceae). Mar Biol 115(3):373–380. Scholar
  50. Durako MJ, Hall MO (1992) Effects of light on the stable carbon isotope composition of the seagrass Thalassia testudinum. Mar Ecol Prog Ser 86:99–101CrossRefGoogle Scholar
  51. Ellison AM, Bank MS, Clinton BD et al (2005) Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Front Ecol Environ 3:479–486CrossRefGoogle Scholar
  52. Ehlers A, Worm B, Reusch TBH (2008) Importance of genetic diversity in eelgrass Zostera marina for its resilience to global warming. Mar Ecol Prog Ser 355:1–7Google Scholar
  53. Erftemeijer PLA, Lewis RRR (2006) Environmental impacts of dredging on seagrasses: a review. Mar Pollut Bull 52:1553–1572CrossRefPubMedGoogle Scholar
  54. Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath G, Okazaki R, Muehllehner N, Glas MN, Lough JM (2011) Losers and winners in coral reefs acclimated to elevated carbon dioxide concentrations. Nat Clim Change 1:165–169. Scholar
  55. Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414–432CrossRefGoogle Scholar
  56. Feng M, McPhaden MJ, Xie S-P, Hafner J (2013) La Niña forces unprecedented Leeuwin Current warming in 2011. Sci Rep 3:1277CrossRefPubMedPubMedCentralGoogle Scholar
  57. Fourqurean JW, Zieman JC (1991) Photosynthesis, respiration and whole plant carbon budget of the seagrass Thalassia testudinum. Mar Ecol Prog Ser 69:161–170CrossRefGoogle Scholar
  58. Fourqurean JW, Duarte CM, Kennedy H, Marba N, Holmer M, Mateo MA, Apostolaki ET, Kendrick GA, Krause-Jensen D, McGlathery KJ, Serrano O (2012) Seagrass ecosystems as a globally significant carbon stock. Nat Geosci 5(7):505–509. Scholar
  59. Frankignoulle M, Bouquegneau JM (1990) Daily and yearly variations of total inorganic carbon in a productive coastal area. Estuar Coast Shelf Sci 30:79–89CrossRefGoogle Scholar
  60. Frankignoulle M, Distèche A (1984) CO2 chemistry in the water column above a Posidonia seagrass bed and related air-sea exchanges. Oceanol Acta 7:209–219Google Scholar
  61. Fraser MW, Kendrick GA, Statton J, Hovey RK, Perez AZ, Walker DI (2014) Extreme climate events lower resilience of foundation seagrass at edge of biogeographical range. J Ecol 102(6):1528–1536CrossRefGoogle Scholar
  62. Frieder CA, Nam SH, Martz TR, Levin LA (2012) High temporal and spatial variability of dissolved oxygen and pH in a nearshore California kelp forest. Biogeosciences 9(10):3917–3930. Scholar
  63. Gattuso JP, Hansson L (2011) Ocean acidification: background and history. In: Gattuso JP, Hansson L (eds) Ocean acidification. Oxford University Press, Oxford, pp 1–16Google Scholar
  64. Gordillo FJL, Figueroa FL, Niell FX (2003) Photon- and carbon-use efficient in Ulva rigida at different CO2 and N levels. Planta 218:315–322. Scholar
  65. Granata TC, Serra T, Colomer J, Casamitjana X, Duarte CM, Gacia E (2001) Flow and particle distributions in a nearshore seagrass meadow before and after a storm. Mar Ecol Prog Ser 218:95–106. Scholar
  66. Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia M-C (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454(7200):96–99. Scholar
  67. Hansen J, Sato M, Ruedy R, Lo K, Lea DW, Medina-Elizade M (2006) Global temperature change. Proc Natl Acad Sci USA 103(39):14288–14293. Scholar
  68. Harley CD, Randall Hughes A, Hultgren KM et al (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241CrossRefPubMedGoogle Scholar
  69. Hawkins SJ, Moore PJ, Burrows MT et al (2008) Complex interactions in a rapidly changing world: responses of rocky shore communities to recent climate change. Clim Res 37:123–133CrossRefGoogle Scholar
  70. Hellblom F, Axelsson L (2003) External HCO3 dehydration maintained by acid zones in the plasma membrane is an important component of the photosynthetic carbon uptake in Ruppia cirrhosa. Photosynth Res 77(2–3):173–181. Scholar
  71. Hemminga MA, Mateo MA (1996) Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Mar Ecol Prog Ser 140:285–298CrossRefGoogle Scholar
  72. Hendriks IE, Sintes T, Bouma TJ, Duarte CM (2008) Experimental assessment and modeling evaluation of the effects of the seagrass Posidonia oceanica on flow and particle trapping. Mar Ecol Prog Ser 356:163–173. Scholar
  73. Hendriks IE, Olsen YS, Ramajo L, Basso L, Steckbauer A, Moore TS, Howard J, Duarte CM (2014) Photosynthetic activity buffers ocean acidification in seagrass meadows. Biogeosciences 11(2):333–346. Scholar
  74. Hepburn CD, Pritchard DW, Cornwall CE, McLeod RJ, Beardall J, Raven JA, Hurd CL (2011) Diversity of carbon use strategies in a kelp forest community: implications for a high CO2 ocean. Glob Change Biol 17(7):2488–2497. Scholar
  75. Hillman K, McComb AJ, Walker DI (1995) The distribution, biomass and primary production of the seagrass Halophila ovalis in the Swan/Canning Estuary, Western Australia. Aquat Bot 51:1–54CrossRefGoogle Scholar
  76. Hobday AJ, Pecl GT (2014) Identification of global marine hotspots: sentinels for change and vanguards for adaptation action. Rev Fish Biol Fish 24(2):415–425. Scholar
  77. Hofmann GE, Barry JP, Edmunds PJ, Gates RD, Hutchins DA, Klinger T, Sewell MA (2010) The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism-to-ecosystem perspective. Annu Rev Ecol Evol Syst 41:127–147. Scholar
  78. Hofmann GE, Smith JE, Johnson KS, Send U, Levin LA, Micheli F, Paytan A, Price NN, Peterson B, Takeshita Y, Matson PG, Crook ED, Kroeker KJ, Gambi MC, Rivest EB, Frieder CA, Yu PC, Martz TR (2011) High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS ONE 6(12):e28983. Scholar
  79. Hofmann L, 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(1):231–242. Scholar
  80. Invers O, Romero J, Pérez M (1997) Effects of pH on seagrass photosynthesis: a laboratory and field assessment. Aquat Bot 59:185–194CrossRefGoogle Scholar
  81. Invers O, Zimmerman RC, Alberte RS, Perez M, Romero J (2001) Inorganic carbon sources for seagrass photosynthesis: an experimental evaluation of bicarbonate use in species inhabiting temperate waters. J Exp Mar Biol Ecol 265(2):203–217. Scholar
  82. Irving AD, Connell SD, Russell BD (2011) Restoring coastal plants to improve global carbon storage: reaping what we sow. PloS one 6(3):e18311. Scholar
  83. Jackson JBC, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury RH, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293(5530):629–637CrossRefPubMedGoogle Scholar
  84. Jiang ZJ, Huang X-P, Zhang J-P (2010) Effects of CO2 enrichment on photosynthesis, growth, and biochemical composition of seagrass Thalassia hemprichii (Ehrenb.) Aschers. J Integr Plant Biol 52(10):904–913. Scholar
  85. Kendrick GA, Fourqurean JW, Fraser MW, Heithaus MR, Jackson G, Friedman K, Hallac D (2012) Science behind management of Shark Bay and Florida Bay, two P-limited subtropical systems with different climatology and human pressures. Mar Freshw Res 63:941–951CrossRefGoogle Scholar
  86. Kilminster K, McMahon K, Waycott M, Kendrick GA, Scanes P, McKenzie L, O’Brien KR, Lyons M, Ferguson A, Maxwell P, Glasby T, Udy J (2015) Unravelling complexity in seagrass systems for management: Australia as a microcosm. Sci Total Environ 534:97–109. Scholar
  87. Kleypas JA, Anthony KRN, Gattuso J-P (2011) Coral reefs modify their seawater carbon chemistry—case study from a barrier reef (Moorea, French Polynesia). Glob Change Biol 17(12):3667–3678. Scholar
  88. Koch M, Bowes G, Ross C, Zhang XH (2013) Climate change and ocean acidfication effects on seagrasses and marine macroalgae. Glob Change Biol 19:103–132. Scholar
  89. Koutalianou M, Orfanidis S, Katsaros C (2015) Effects of high temperature on the ultrstructure and micrtubule organisation of interphase and dividing cells of the seagrass Cymodocea nodosa. Protoplasma. Scholar
  90. 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(11):1419–1434. Scholar
  91. Larkum A, Roberts G, Kuo J, Strother S (1989) Gaseous Movement in Seagrasses. Biology of seagrasses. A treatise on the biology of seagrasses with special reference to the Australian region. Elsevier Science Publishers, Amsterdam, pp 686–722Google Scholar
  92. Last PR, White WT, Gledhill DC, Hobday AJ, Brown R, Edgar GJ, Pecl G (2011) Long-term shifts in abundance and distribution of a temperate fish fauna: a response to climate change and fishing practices. Glob Ecol Biogeogr 20(1):58–72. Scholar
  93. Lee K-S, Park SR, Kim YK (2007) Effects of irradiance, temperature, and nutrients on growth dynamics of seagrasses: a review. J Exp Mar Biol Ecol 350:144–175Google Scholar
  94. Levitus S, Antonov JI, Wang JL, Delworth TL, Dixon KW, Broccoli AJ (2001) Anthropogenic warming of Earth’s climate system. Science 292(5515):267–270. Scholar
  95. Lough JM (2012) Small change, big difference: sea surface temperature distributions for tropical coral reef ecosystems, 1950–2011. J Geophys Res-Oceans 117.
  96. Madsen TV, Sand-Jensen K (1991) Photosynthetic carbon assimilation in aquatic macrophytes. Aquat Bot 41:5–40. Scholar
  97. Manzello DP, Enochs IC, Melo N, Gledhill DK, Johns EM (2012) Ocean acidification refugia of the Florida reef tract. PloS one 7(7):e41715. Scholar
  98. Marbà N, Walker DI (1999) Growth, flowering, and population dynamics of temperate Western Australian seagrasses. Mar Ecol Prog Ser 184:105–118CrossRefGoogle Scholar
  99. Marbà N, Duarte CM (2010) Mediterranean warming triggers seagrass (Posidonia oceanica) shoot mortality. Global Change Biol 16:2366–2375Google Scholar
  100. Masini RJ, Cary JL, Simpson CJ, McComb AJ (1995) Effects of light and temperature on the photosynthesis of meadow-forming seagrasses in Western Australia. Aquat Bot 49:239–254Google Scholar
  101. Massa SI, Pearson GA, Aires T, Kube M, Olsen JL, Reinhardt R, Serrão EA, Arnaud-Haond S (2011) Expressed sequence tags from heat-shocked seagrass Zostera noltii (Hornemann) from its southern distribution range. Mar Genomics 4(3):181–188Google Scholar
  102. McKenzie LJ, Collier CJ, Langlois LA, Yoshida RL, Smith N, Takahashi M, Waycott M (2015) Marine monitoring program: inshore seagrass. Annual report for the sampling period 1st June 2013–31st May 2014. TropWATER, James Cook University, Cairns, AustraliaGoogle Scholar
  103. McMahon KM (2005) Recovery of subtropical seagrasses from natural disturbance. The University of Queensland, BrisbaneGoogle Scholar
  104. Meehl GA, Stocker TF (2007) Global climate projections. Climate Change 2007: The Physical Science BasisGoogle Scholar
  105. Mellors JE (2003) Sediment and nutrient dynamics in coastal intertidal seagrass of north eastern tropical Australia. Ph.D. thesis, James Cook University, Australia, James Cook University, AustraliaGoogle Scholar
  106. Mellors J, Waycott M, Marsh H (2005) Variation in biogeochemical parameters across intertidal seagrass meadows in the central Great Barrier Reef region. Mar Poll Bull 51:335–342CrossRefGoogle Scholar
  107. Mercado JM, Gordillo FJL (2011) Inorganic carbon acquisition in algal communities: are the laboratory data relevant to the natural ecosystems? Photosynth Res 109(1–3):257–267. Scholar
  108. Mercado J, Niell FX, Silva J, Santos R (2003) Use of light and inorganic carbon acquisition by two morphotypes of Zostera noltii Hornem. J Exp Mar Biol Ecol 297:71–84CrossRefGoogle Scholar
  109. Millar AH, James W, Soole KL, Day DA (2011) The organisation and regulation of mitochondrial respiration in plants. Annu rev plant biol 61(1):79–104Google Scholar
  110. Morse JW, Zullig JJ, Iverson RL, Choppin GR, Mucci A, Millero FJ (1987) The influence of seagrass beds on carbonate sediment in the Bahamas. Mar Chem 22:71–83CrossRefGoogle Scholar
  111. Olsen YS, Sánchez-Camacho M, Marbà N, Duarte CM (2012) Mediterranean seagrass growth and demography responses to experimental warming. Estuaries Coasts 35(5):1205–1213. Scholar
  112. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner GK, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig MF, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437(7059):681–686. Scholar
  113. Ow YX, Collier CJ, Uthicke S (2015) Responses of three tropical seagrass species to CO2 enrichment. Mar Biol 162(5):1005–1017. Scholar
  114. Ow YX, Uthicke S, Collier CJ (2016a) Light levels affect carbon utilisation in tropical seagrass under ocean acidification. PLoS ONE 11(3):e0150352. Scholar
  115. Ow YX, Vogel N, Collier CJ, Holtum JA, Flores F, Uthicke S (2016b) Nitrate fertilisation does not enhance CO2 responses in two tropical seagrass species. Sci Rep 6:23093. Scholar
  116. Palacios SL, Zimmerman RC (2007) Response of eelgrass Zostera marina to CO2 enrichment: possible impacts of climate change and potential for remediation of coastal habitats. Mar Ecol Prog Ser 344:1–13. Scholar
  117. Pearce AF, Feng M (2013) The rise and fall of the “marine heat wave” off Western Australia during the summer of 2010/2011. J Mar Syst 111–112:139–156. Scholar
  118. Pedersen O, Colmer TD, Borum J, Zavala-Perez A, Kendrick GA (2016) Heat stress of two tropical seagrass species during low tides—impact on underwater net photosynthesis, dark respiration and diel in situ internal aeration. New Phytol 210(4):1207–1218. Scholar
  119. Perez MP, Romero J (1992) Photosynthetic response to light and temperature of the seagrass Cymodocea nodosa and the prediction of its seasonality. Aquat Bot 43:51–62Google Scholar
  120. Ralph PJ (1998) Photosynthetic response of laboratory-cultured Halophila ovalis to thermal stress. Mar Ecol Prog Ser 171:123–130Google Scholar
  121. Raven JA, Walker DI, Johnston AM, Handley LL, Kübler JE (1995) Implications of 13C natural abundance measurements for photosynthetic performance by marine macrophytes in their natural environment. Mar Ecol Prog Ser 123:193–205CrossRefGoogle Scholar
  122. 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 29:355–378CrossRefGoogle Scholar
  123. Raven JA, Caldeira K, Elderfield H, Hoegh-Guldberg O, Liss P, Riebesell U, Shepherd J, Turkey C, Watson A, Heap R, Banes R, Quinn R (2005) Ocean acidification due to increasing atmospheric carbon dioxide. The Royal Society, The Clyvedon Press Ltd., CardiffGoogle Scholar
  124. Reynolds LK, DuBois K, Abbott JM, Williams SL, Stachowicz JJ (2016) Response of a habitat-forming marine plant to a simulated warming event is delayed, genotype specific and varies with phenology. PLos One 11(6):e0154532.
  125. Romero J, Pérez M, Mateo MA, Sala E (1994) The belowground organs of the Mediterranean seagrass Posidonia oceanica as a biogeochemical sink. Aquat Bot 47:13–19Google Scholar
  126. Romero J, Lee KS, Perez M, Mateo MA, Alcoverro T (2006) Nutrient dynamics in seagrass ecosystems. In: Larkum AWD, Orth RJ, Duarte C (eds) Seagrasses: biology, ecology and conservation, vol XVI. Springer, The Netherlands, pp 227–254Google Scholar
  127. Rose TH, Smale DA, Botting G (2012) The 2011 marine heat wave in Cockburn Sound, southwest Australia. Ocean Sci 8(4):545–550. Scholar
  128. Russell BD, Thompson JI, Falkenberg LJ, Connell SD (2009) Synergistic effects of climate change and local stressors: CO2 and nutrient-driven change in subtidal rocky habitats. Glob Change Biol 15:2153–2162. Scholar
  129. Russell BD, Connell SD, Uthicke S, Muehllehner N, Fabricius KE, Hall-Spencer JM (2013) Future seagrass beds: can increased productivity lead to increased carbon storage? Mar Pollut Bull. Scholar
  130. 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, Oxfordshire, UK, pp 31–49Google Scholar
  131. Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R, Wong CS, Wallace DWR, Tilbrook B, Millero FJ, Peng TH, Kozyr A, Ono T, Rios AF (2004) The oceanic sink for anthropogenic CO2. Science 305(5682):367–371. Scholar
  132. Salvucci ME, Crafts-Brandner SJ (2004) Relationship between the heat tolerance of photosynthesis and the thermal stability of rubisco activase in plants from contrasting environments. Plant Physiol 134(4):1460–1470Google Scholar
  133. Sand-Jensen K, Gordon DM (1984) Differential ability of marine and freshwater macrophytes to utilize HCO3 and CO2. Mar Biol 80(3):247–253. Scholar
  134. Scheible WR, Gonzalez-Fontes A, Lauerer M, Muller-Rober B, Caboche M, Stitt M (1997) Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in Tobacco. Plant Cell 9(5):783–798. Scholar
  135. Schmalz RF, Swanson FJ (1969) Diurnal variations in the carbonate saturation of seawater. J Sediment Petrol 39:255–267Google Scholar
  136. Schwarz AM, Bjork M, Buluda T, Mtolera H, Beer S (2000) Photosynthetic utilisation of carbon and light by two tropical seagrass species as measured in situ. Mar Biol 137(5–6):755–761. Scholar
  137. Semesi IS, Beer S, Björk M (2009) Seagrass photosynthesis controls rates of calcification and photosynthesis of calcareous macroalgae in a tropical seagrass meadow. Mar Ecol Prog Ser 382:41–48. Scholar
  138. Short FT, Neckles HA (1999) The effects of global climate change on seagrasses. Aquat Bot 63:169–196Google Scholar
  139. Sinclair EA, Statton J, Hovey R, Anthony J, Dixon KW, Kendrick GA (2016) Reproduction at the extremes: pseudovivipary, hybridization, and genetic mosaicism in Posidonia australis (Posidoniaceae). Ann Bot 117:237–247PubMedGoogle Scholar
  140. Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (2007) Contribution of working group 1 to the fourth assessment report of the IPCC. Cambridge, UKGoogle Scholar
  141. Staehr PA, Borum J (2011) Seasonal acclimation in metabolism reduces light requirements of eelgrass (Zostera marina). J Exp Mar Biol Ecol 407(2):139–146.
  142. Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 22:583–621. Scholar
  143. Takahashi M, Noonan SHC, Fabricius KE, Collier CJ (2015) The effects of long-term in situ CO2 enrichment on tropical seagrass communities at volcanic vents. ICES J Mar Sci: J Conseil. Scholar
  144. Thomson J, Burkholder D, Heithaus M, Fourqurean J, Fraser M, Statton J, Kendrick GA (2015) Extreme temperatures, foundation species and abrupt ecosystem shifts: an example from an iconic seagrass ecosystem. Glob Change Biol 21:1463–1474CrossRefGoogle Scholar
  145. Touchette BW, Burkholder JM (2000) Overview of the physiological ecology of carbon metabolism in seagrasses. J Exp Mar Biol Ecol 250:169–205. Scholar
  146. Touchette BW, Burkholder JM (2007) Carbon and nitrogen metabolism in the seagrass, Zostera marina L.: environmental control of enzymes involved in carbon allocation and nitrogen assimilation. J Exp Mar Biol Ecol 350:216–233CrossRefGoogle Scholar
  147. Udy JW, Dennison WC, Long WJL, McKenzie LJ (1999) Responses of seagrass to nutrients in the Great Barrier Reef, Australia. Mar Ecol Prog Ser 185:257–271CrossRefGoogle Scholar
  148. Uku J, Beer S, Björk M (2005) Buffer sensitivity of photosynthetic carbon utilisation in eight tropical seagrasses. Mar Biol 147:1085–1090CrossRefGoogle Scholar
  149. Unsworth RKF, Collier CJ, Henderson GM, McKenzie LJ (2012) Tropical seagrass meadows modify seawater carbon chemistry: implications for coral reefs impacted by ocean acidification. Environ Res Lett 7(2):024026. Scholar
  150. Unsworth RKF, Collier CJ, Waycott M, McKenzie LJ, Cullen-Unsworth LC (2015) A framework for the resilience of seagrass ecosystems. Mar Pollut Bull 100(1):34–46. Scholar
  151. Uthicke S, Furnas M, Lønborg C (2014) Coral reefs on the edge? Carbon chemistry on inshore reefs of the Great Barrier Reef. PLoS ONE 9:e109092CrossRefPubMedPubMedCentralGoogle Scholar
  152. van Dongen JT, Gupta KJ, Ramírez-Aguilar SJ, Araújo WL, Nunes-Nesi A, Fernie AR (2011) Regulation of respiration in plants: a role for alternative metabolic pathways. J Plant Physiol 168(12):1434–1443CrossRefPubMedGoogle Scholar
  153. Walker DI, Kendrick GA, McComb AJ (1988) The distribution of seagrass species in Shark Bay, Western Australia, with notes on their ecology. Aquat Bot 30:305–317CrossRefGoogle Scholar
  154. Walker DI, Dennison WC, Edgar G (1999) Status of Australian seagrass research and knowledge. In: Butler A, Jernakoff P (eds) Seagrass in Australia. CSIRO Australia, Collingwood, pp 1–18Google Scholar
  155. Waycott M, McMahon K, Mellors J, Calladine A, Kleine D (2004) A guide to tropical seagrasses of the Indo-West Pacific. James Cook University, TownsvilleGoogle Scholar
  156. Wernberg T, Russell BD, Thomsen MS, Gurgel CFD, Bradshaw CJA, Poloczanska ES, Connell SD (2011) Seaweed communities in retreat from ocean warming. Curr Biol 21(21):1828–1832. Scholar
  157. Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ, de Bettignies T, Bennett S, Rousseaux CS (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat Clim Change 3:78–82CrossRefGoogle Scholar
  158. Wernberg T, Bennett S, Babcock RC, de Bettignies T, Cure K, Depczynski M, Dufois F, Fromont J, Fulton CJ, Hovey RK, Harvey ES, Holmes TH, Kendrick GA, Radford B, Santana-Garcon J, Saunders BJ, Smale DA, Thomsen MS, Tuckett CA, Tuya F, Vanderklift MA, Wilson S (in press) Climate driven phase shift of a temperate marine ecosystem. Science (Accepted 31st May 2016), aad8745Google Scholar
  159. Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C3, C4 and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res 119(1–2):102–117Google Scholar
  160. York PH, Gruber RK, Hill R, Ralph PJ, Booth DJ, Macreadie PI (2013) Physiological and morphological responses of the temperate seagrass Zostera muelleri to multiple stressors: investigating the interactive effects of light and temperature. PLoS ONE 8(10):e76377.
  161. Zimmerman RC, Kohrs DG, Steller DL, Alberte RS (1997) Impacts of CO2 enrichment on productivity and light requirements of eelgrass. Plant Physiol 115:599–607CrossRefPubMedPubMedCentralGoogle Scholar
  162. Zou DH, Gao KS (2009) Effects of elevated CO2 on the red seaweed Gracilaria lemaneiformis (Gigartinales, Rhodophyta) grown at different irradiance levels. Phycologia 48:510–517. Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Ylva S. Olsen
    • 1
    Email author
  • Catherine Collier
    • 2
    • 3
  • Yan X. Ow
    • 4
  • Gary A. Kendrick
    • 1
  1. 1.School of Biological Sciences and the Oceans InstituteThe University of Western AustraliaCrawleyAustralia
  2. 2.College of Marine and Environmental SciencesJames Cook UniversityTownsvilleAustralia
  3. 3.Centre for Tropical Water and Aquatic Ecosystem Research (TropWATER)James Cook UniversityCairnsAustralia
  4. 4.Experimental Marine Ecology Laboratory, Department of Biological SciencesNational University of SingaporeSingaporeSingapore

Personalised recommendations