Effects of ocean acidification on Posidonia oceanica epiphytic community and shoot productivity

Journal of Ecology

Volumn 103, Issue 6, 2015, Pages 1594-1609

  Cox, T Erin ^a   Schenone, Stefano ^a,b   Delille, Jeremy ^a   Díaz Castañeda, Victoria ^c   Alliouane, Samir ^a   Gattuso, Jean Pierre ^a,d   Gazeau, Frédéric ^a  

^a LABORATOIRE D OCÉANOGRAPHIE DE VILLEFRANCHE   (France)

^b UNIVERSITY OF GENOA   (Italy)

^c CENTRO DE INVESTIGACIÓN CIENTÍFICA Y DE EDUCACIÓN SUPERIOR DE ENSENADA   (Mexico)

^d SCIENCES PO   (France)

Author keywords

pH; Posidonia oceanica; Calcified growth; Carbon dioxide; Climate change; Coralline algae; Net calcification; Photosynthesis; Plant climate interactions; Seagrass epiphyte interactions

Indexed keywords

ACIDIFICATION; ATMOSPHERE-BIOSPHERE INTERACTION; CALCIFICATION; CARBON DIOXIDE; CHLOROPHYLL; CLIMATE CHANGE; COMMUNITY RESPONSE; EPIPHYTE; GROWTH RESPONSE; NET ECOSYSTEM PRODUCTION; PH; PHOTOSYNTHESIS; RED ALGA; RESPIRATION; SEAGRASS; SHOOT;

ALGAE; INVERTEBRATA; POSIDONIA; POSIDONIA OCEANICA;

EID: 84944474782     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/1365-2745.12477     Document Type: Article

References (93)

1. Agostini, S., Desjobert, J.M. & Pergent, G. (1998) Distribution of phenolic compounds in Posidonia oceanica. Phytochemistry, 48, 611-617.
2. Alcoverro, T., Duarte, C.M. & Romero, J. (1995) Annual growth dynamics of Posidonia oceanica: contribution of large-scale versus local factors to seasonality. Marine Ecology Progress Series, 120, 203-210.
3. Alcoverro, T., Manzanera, M. & Romero, J. (1998) Seasonal and age-dependent variability of Posidonia oceanica (L.) Delile photosynthetic parameters. Journal of Experimental Marine Biology and Ecology., 230, 1-13.
4. Alcoverro, T., Manzanera, M. & Romero, J. (2001) Annual metabolic carbon balance of the seagrass Posidonia oceanica: the importance of carbohydrate reserves. Marine Ecology Progress Series, 211, 105-116.
5. 2 in a Mediterranean volcanic vent. Marine Environmental Research, 99, 9-15.
6. Arnold, T., Mealey, C., Leahey, H., Miller, A.W., Hall-Spencer, J.M., Milazzo, M. & Maers, K. (2012) Ocean acidification and the loss of phenolic substances in marine plants. PLoS One, 7, e35107.
7. Asnaghi, V., Chiantore, M., Mangialajo, L., Gazeau, F., Francour, P., Alliouane, S. & Gattuso, J.-P. (2013) Cascading effects of ocean acidification in a rocky subtidal community. PLoS One, 8, e61978.
8. 2 levels. Annual Review of Ecology and Systematics, 21, 167-196.
9. Beer, S. & Björk, M. (2000) Measuring rates of photosynthesis of two tropical seagrasses by pulse amplitude modulated (PAM) fluorometry. Aquatic Botany, 66, 69-76.
10. Borowitzka, M.A., Lavery, P.S. & van Keulen, M. (2006) Seagrasses: biology, ecology and conservation. Epiphytes of Seagrasses (eds A.W.D. Larkum, R.J. Orth & C.M. Duarte), pp. 441-461. Springer, Dordrecht, The Netherlands.
11. Bosence, D. (1989) Biogenic carbonate production in Florida Bay. Bulletin of Marine Science, 44, 419-433.
12. Buapet, P., Rasmusson, L.M., Gullstrom, M., Bjork, M., Gullström, M. & Björk, M. (2013) Photorespiration and carbon limitation determine productivity in temperate seagrasses. PLoS One, 8, 1-9.
13. 2 contingent on epiphytic algae: indirect effects can overwhelm direct effects. Oecologia, 176, 871-882.
14. Campbell, J.E. & Fourqurean, J.W. (2013) Mechanisms of bicarbonate use influence the photosynthetic carbon dioxide sensitivity of tropical seagrasses. Limnology and Oceanography, 58, 839-848.
15. Campbell, J.E. & Fourqurean, J.W. (2014) Ocean acidification outweighs nutrient effects in structuring seagrass epiphyte communities. Journal of Ecology, 102, 730-737.
16. Cebrián, J., Enríquez, S., Fortes, M.D., Agawin, N., Vermaat, J.E. & Duarte, C.M. (1999) Epiphyte accrual on Posidonia oceanica (L.) Delile leaves: implications for light absorption. Botanica Marina, 42, 123-128.
17. Ciais, P., Sabine, C., Bala, G., Bopp, L., Brovkin, V., Canadell, J. et al. (2013) Carbon and Other Biogeochemical Cycles. Cambridge University Press, Cambridge, UK and New York, NY, USA.
18. Connell, S.D., Russell, B.D. & Irving, A.D. (2011) Can strong consumer and producer effects be reconciled to better forecast "catastrophic" phase-shifts in marine ecosystems? Journal of Experimental Marine Biology and Ecology, 400, 296-301.
19. 2 as a resource among competitors for ecosystem dominance. Philosophical Transactions of the Royal Society B: Biological Sciences, 368, 20120442-20120442.
20. Cornelisen, C.D. & Thomas, F.I. (2002) Ammonium uptake by seagrass epiphytes: isolation of the effects of water velocity using an isotope label. Limnology and Oceanography, 47, 1223-1229.
21. Costanza, R., D'Arge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B. et al. (1997) The value of the world's ecosystem services and natural capital. Ecological Economics, 387, 253-260.
22. Diaz-Pulido, G., McCook, L.J., Dove, S., Berkelmans, R., Roff, G., Kline, D.I., Weeks, S., Evans, R.D., Williamson, D.H. & Hoegh-Guldberg, O. (2009) Doom and boom on a resilient reef: climate change, algal overgrowth and coral recovery. PLoS One, 4, e5239.
23. 2 Measurements. PICES Special Publication 3, British Columbia, Canada.
24. Duarte, C.M. (1990) Seagrass nutrient content. Marine Ecology Progress Series, 67, 201-207.
25. Duarte, C.M. & Chiscano, C.L. (1999) Seagrass biomass and production: a reassessment. Aquatic Botany, 65, 159-174.
26. Duarte, C.M., Marba, N., Gacia, E., Fourqurean, J.W., Beggins, J., Barron, C. & Apostolaki, E.T. (2010) Seagrass community metabolism: assessing the carbon sink capacity of seagrass meadows. Global Biogeochemical Cycles, 24, 1-9.
27. Fabricius, K.E., Langdon, C., Uthicke, S., Humphrey, C., Noonan, S., De'ath, G., Okazaki, R., Muehllehner, N., Glas, M.S. & Lough, J.M. (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nature Climate Change, 1, 165-169.
28. Farmer, A. (1990) The effects of lake acidification on aquatic macrophytes - a review. Environmental Pollution, 65, 219-240.
29. Garrard, S.L., Gambi, M.C., Scipione, M.B., Patti, F.P., Lorenti, M., Zupo, V., Paterson, D.M. & Buia, M.C. (2014) Indirect effects may buffer negative responses of seagrass invertebrate communities to ocean acidification. Journal of Experimental Marine Biology and Ecology, 461, 31-38.
30. 2 enrichment (FOCE) systems: present status and future developments. Biogeosciences, 11, 4057-4075.
31. Genty, B., Briantais, J.-M. & Baker, N.R. (1989) The relationship between the quantum yield of photosynthetic electron transport and photochemical quenching of chlorophyll fluorescence. Biochemical Biophysical Acta, 990, 87-92.
32. Gobert, S., Laumont, N. & Bouquegneau, J.-M. (2002) Posidonia oceanica meadow: a low nutrient high chlorophyll (LNHC) system? BMC Ecology, 2, 9.
33. Gobert, S., Cambridge, M.L., Velimirov, B., Pergent, G., Lepoint, G., Bouquegneau, J.-M., Duaby, P., Pergent-Martini, C. & Walker, D.I. (2006) Biology of Posidonia. Seagrasses: Biology, Ecology and Conservation (eds A.W.D. Larkum, R.J. Orth & C.M. Duarte), pp. 387-408. Springer, Dordrecht, The Netherlands.
34. Goering, J.J. & Parker, P.L. (1972) Nitrogen fixation by epiphytes on sea grasses. Limnology and Oceanography, 17, 320-323.
35. Gorsky, G., Ohman, M.D., Picheral, M., Gasparini, S., Stemmann, L., Romagnan, J.B., Cawood, A., Pesant, S., Garcia-Comas, C. & Prejger, F. (2010) Digital zooplankton image analysis using the ZooScan integrated system. Journal of Plankton Research, 32, 285-303.
36. Hall-Spencer, J.M., Rodolfo-Metalpa, R., Martin, S., Ransome, E., Fine, M., Turner, S.M., Rowley, S.J., Tedesco, D. & Buia, M.C. (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature, 454, 96-99.
37. Harlin, M.M. (1975) Epiphyte-host relations in seagrass communities. Aquatic Botany, 1, 125-131.
38. Heck, K.L. & Valentine, J.F. (2006) Plant-herbivore interactions in seagrass meadows. Journal of Experimental Marine Biology and Ecology, 330, 420-436.
39. Hendriks, I.E., Olsen, Y.S., Ramajo, L., Basso, L., Steckbauer, A., Moore, T.S., Howard, J. & Duarte, C.M. (2013) Photosynthetic activity buffers ocean acidification in seagrass meadows. Biogeosciences Discussions, 10, 12313-12346.
40. Hendriks, I.E., Duarte, C.M., Olsen, Y.S., Steckbauer, A., Ramajo, L., Moore, T.S., Trotter, J.A. & McCulloch, M. (2014) Biological mechanisms supporting adaptation to ocean acidification in coastal ecosystems. Estuarine Coastal and Shelf Science, 152, 1-8.
41. Hofmann, L.C. & Bischof, K. (2014) Ocean acidification effects on calcifying macroalgae. Aquatic Biology, 22, 261-279.
42. Hurd, C.L. (2015) Slow-flow habitats as refugia for coastal calcifiers from ocean acidification. Journal of Phycology, 51, 599-605.
43. 2-enriched ocean. Oceanography, 22, 128-145.
44. Invers, O., Romero, J., Perez, M. & Pérez, M. (1997) Effects of pH on seagrass photosynthesis: a laboratory and field assessment. Aquatic Botany, 59, 185-194.
45. Invers, O., Zimmerman, R., Alberte, R.S., Perez, M. & Romero, J. (2001) Inorganic carbon sources for seagrass photosynthesis: an experimental evaluation of bicarbonate use in species inhabiting temperate waters. Journal of Experimental Marine Biology and Ecology, 265, 203-217.
46. 2 availability on the depth distribution of the seagrass Posidonia oceanica (L.) Delile: a tentative assessment using a carbon balance model. Bulletin of Marine Science, 71, 1191-1198.
47. Jassby, A.D. & Platt, T. (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnology and Oceanography, 21, 540-547.
48. Jeffrey, S. & Humphrey, G. (1975) New spectrophotometric equations for the determination of chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochemical Physiology Pflanzen, 167, 191-194.
49. 2 enrichment on photosynthesis, growth, and biochemical composition of seagrass Thalassia hemprichii (Ehrenb.) Aschers. Journal of Integrative Plant Biology, 52, 904-913.
50. 2 vent for ocean acidification studies. Estuarine Coastal and Shelf Science, 94, 129-137.
51. Koch, M., Bowes, G., Ross, C. & Zhang, X.H. (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biology, 19, 103-132.
52. Korner, C. (2003) Ecological impacts of atmospheric CO2 enrichment on terrestrial ecosystems. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, 361, 2023-2041.
53. Krause-Jensen, D., Almela, E.D., Cunha, A.H. & Greve, T.M. (2004) Have seagrass abundance and distribution changed? European Seagrasses, an Introduction to Monitoring and Management. (eds J. Borum, C.M. Duarte, D. Krause-Jensen & T.M. Greve), The M&MS project, pp. 30-40. The M & MS project, Copenhagen, Denmark.
54. Kroeker, K.J., Kordas, R.L., Crim, R., Hendriks, I.E., Ramajo, L., Singh, G.S., Duarte, C.M. & Gattuso, J.P. (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biology, 19, 1884-1896.
55. Lavigne, H., Epitalon, J.M. & Gattuso, J.-P. (2014) seacarb: seawater carbonate chemistry with R. ran.r-project.org/package=seacarb.
56. Lawrence, J. (1975) On the relationship between marine plants and sea urchins. Oceanography and Marine Biology - An Annual Review, 13, 213-286.
57. Le Quéré, C., Peters, G.P., Andres, R.J., Andrew, R.M., Boden, T.A., Ciais, P. et al. (2014) Global carbon budget 2013. Earth Systems Science Data, 6, 235-263.
58. Lee, K.-S., Park, S.R. & Kim, Y.K. (2007) Effects of irradiance, temperature, and nutrients on growth dynamics of seagrasses: a review. Journal of Experimental Marine Biology and Ecology, 350, 144-175.
59. Lepoint, G., Havelange, S., Gobert, S. & Bouquegneau, J.M. (1999) Fauna vs flora contribution to the leaf epiphytes biomass in a Posidonia oceanica seagrass bed (Revellata Bay, Corsica). Hydrobiologia, 394, 63-67.
60. Lepoint, G., Nyssen, F., Gobert, S., Dauby, P. & Bouquegneau, J.M. (2000) Relative impact of a seagrass bed and its adjacent epilithic algal community in consumer diets. Marine Biology, 136, 513-518.
61. Libes, M. (1986) Productivity-irradiance relationship of Posidonia oceanica and its epiphytes. Aquatic Botany, 26, 285-306.
62. Mabrouk, L., Hamza, A., Brahm, M.B., Bradai, M.N. & Bradai, M.N. (2013) Variability in the structure of epiphyte assemblages on leaves and rhizomes of Posidonia oceanica in relation to human disturbances in a seagrass meadow off Tunisia. Aquatic Botany, 108, 33-40.
63. Marbà, N. & Duarte, C.M. (1997) Interannual changes in seagrass (Posidonia oceanica) growth and environmental change in the Spanish Mediterranean littoral zone. Limnology and Oceanography, 42, 800-810.
64. Marbà, N. & Duarte, C.M. (2010) Mediterranean warming triggers seagrass (Posidonia oceanica) shoot mortality. Global Change Biology, 16, 2366-2375.
65. Marbà, N., Hemminga, M.A., Mateo, M.A., Duarte, C.M., Mass, Y.E.M., Terrados, J. & Gacia, E. (2002) Carbon and nitrogen translocation between seagrass ramets. Marine Ecology Progress Series, 226, 287-300.
66. Martin, S. & Gattuso, J.-P. (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Global Change Biology, 15, 2089-2100.
67. Martin, S., Rodolfo-Metalpa, R., Ransome, E., Rowley, S., Buia, M.-C.C., Gattuso, J.-P. & Hall-Spencer, J. (2008) Effects of naturally acidified seawater on seagrass calcareous epibionts. Biology Letters, 4, 689-692.
68. 2 and nutrient-driven changes across multiple levels of organization in Zostera noltii ecosystems. Biogeosciences Discussions, 11, 5239-5274.
69. McCoy, S.J. & Kamenos, N.A. (2015) Coralline algae (Rhodophyta) in a changing world: integrating ecological, physiological, and geochemical responses to global change. Journal of Phycology, 51, 6-24.
70. Morse, J.W. & Mackenzie, F.T. (1990) Geochemistry of Sedimentary Carbonates, pp. 707. Elsevier, Amsterdam.
71. Nelson, W. (2009) Calcified macroalgae - critical to coastal ecosystems and vulnerable to change: a review. Marine and Freshwater Research, 60, 787-801.
72. Orr, J.C., Fabry, V.J. & Aumont, O. (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature, 437, 681-686.
73. Orth, R.J., Carruthers, T.J.B., Dennison, W.C., Duarte, C.M., Fourqurean, J.W., Heck, K.L. et al. (2006) A global crisis for seagrass ecosystems. BioScience, 56, 681-686.
74. 2 enrichment: possible impacts of climate change and potential for remediation of coastal habitats. Marine Ecology Progress Series, 344, 1-13.
75. Peduzzi, P. (1987) Dietary preferences and carbon absorption by two grazing gastropods, Gibbula umbilicaris (Linné) and Jujubinus striatus (Linné). Marine Ecology, 8, 359-370.
76. Pergent, G., Romero, J., Pergent-Martini, C., Mateo, M.A. & Boudouresque, C.F. (1994) Primary production, stocks and fluxes in the Mediterranean seagrass Posidonia oceanica. Marine Ecology Progress Series, 106, 139-146.
77. Perry, C.T. & Beavington-Penney, S.J. (2005) Epiphytic calcium carbonate production and facies development within sub-tropical seagrass beds, Inhaca Island, Mozambique. Sedimentary Geology, 174, 161-176.
78. Piazzi, L., Balata, D., Cinelli, F. & Benedetti-Cecchi, L. (2004) Patterns of spatial variability in epiphytes of Posidonia oceanica: differences between a disturbed and two reference locations. Aquatic Botany, 79, 345-356.
79. Platt, T., Gallegos, C. & Harrison, W. (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. Journal of Marine Research, 38, 687-701.
80. Poore, A.G.B., Graba-Landry, A., Favret, M., Sheppard Brennand, H., Byrne, M. & Dworjanyn, S.A. (2013) Direct and indirect effects of ocean acidification and warming on a marine plant-herbivore interaction. Oecologia, 173, 1113-1124.
81. Prado, P., Alcoverro, T. & Romero, J. (2008) Seasonal response of Posidonia oceanica epiphyte assemblages to nutrient increase. Marine Ecology Progress Series, 359, 89-98.
82. Ralph, P.J. & Gademann, R. (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquatic Botany, 82, 222-237.
83. Romero, J., Lee, K., Marta, P., Mateo, M. & Alcoverro, T. (2006) Nutrient dynamics in seagrass ecosystems. Seagrasses: Biology, Ecology and Conservation (eds A.W.D. Larkum, R.J. Orth & C.M. Duarte), pp. 227-254. Springer, Dordrecht, The Netherlands.
84. 2. PLoS One, 8, e70455.
85. Sand-Jensen, K., Revsbech, N.P. & Jorgensen, B.B. (1985) Microprofiles of oxygen in epiphyte communities on submerged macrophytes. Marine Biology, 89, 55-62.
86. Short, F., Carruthers, T., Dennison, W. & Waycott, M. (2007) Global seagrass distribution and diversity: a bioregional model. Journal of Experimental Marine Biology and Ecology, 350, 3-20.
87. Smith, S. & Key, G. (1975) Carbon dioxide and metabolism in marine environments. Limnology and Oceanography, 20, 493-495.
88. Steel, J.B. & Wilson, B.J. (2003) Which is the phyte in epiphyte? Folia Geobotanica, 38, 97-99.
89. Tomas, F., Turon, X. & Romero, J. (2005) Seasonal and small-scale spatial variability of herbivory pressure on the temperate seagrass Posidonia oceanica. Marine Ecology Progress Series, 301, 95-107.
90. Uku, J., Beer, S. & Björk, M. (2005) Buffer sensitivity of photosynthetic carbon utilisation in eight tropical seagrasses. Marine Biology, 147, 1085-1090.
91. Van Montfrans, J., Wetzel, R. & Orth, R.J. (1984) Epiphyte-grazer relationships in seagrass meadows: consequences for seagrass growth and production. Estuaries, 7, 289-309.
92. Waycott, M., Duarte, C.M., Carruthers, T.J.B., Orth, R.J., Dennison, W.C., Olyarnik, S. et al. (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences of the United States of America, 106, 12377-12381.
93. 2 enrichment on productivity and light requirements of eelgrass. Plant Physiology, 115, 599-607.