CO2 and inorganic nutrient enrichment affect the performance of a calcifying green alga and its noncalcifying epiphyte

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• 作者：Laurie C. Hofmann (1)
  Kai Bischof (1)
  Cecilia Baggini (2)
  Andrew Johnson (3)
  Ketil Koop-Jakobsen (4) (5)
  Mirta Teichberg (6)
  
  1. Marine Botany ; Bremen Marine Ecology Centre for Research and Education ; University of Bremen ; Leobener Str. NW2 ; 28359 ; Bremen ; Germany
  2. Marine Biology and Ecology Research Center ; Plymouth University ; Plymouth ; Devon ; PL4 8AA ; UK
  3. Department of Biological Sciences ; Virginia Institute of Marine Science ; College of William and Mary ; 1375 Greate Road ; Gloucester Point ; VA ; 23062 ; USA
  4. HGF-MPG Group for Deep-Sea Ecology and Technology ; Max Planck Institute for Marine Microbiology ; Celsiusstra脽e 1 ; 28359 ; Bremen ; Germany
  5. Center for Marine Environmental Sciences ; Leobener Str. ; 28359 ; Bremen ; Germany
  6. Leibniz Center for Tropical Marine Ecology ; Fahrenheitstr. 6 ; 28359 ; Bremen ; Germany
  
• 关键词：Halimeda opuntia ; Dictyota ; Calcification ; Ocean acidification ; Eutrophication
• 刊名：Oecologia
• 出版年：2015
• 出版时间：April 2015
• 年：2015
• 卷：177
• 期：4
• 页码：1157-1169
• 全文大小：892 KB
• 参考文献：1. Beach, K, Walters, L, Borgeas, H, Smith, C, Coyer, J, Vroom, P (2003) The impact of Dictyota spp. on Halimeda populations of Conch Reef, Florida Keys. J Exp Mar Biol Ecol 297: pp. 141-159 CrossRef
  2. Belliveau, SA, Paul, VJ (2002) Effects of herbivory and nutrients on the early colonization of crustose coralline and fleshy algae. Mar Ecol Prog Ser 232: pp. 105-114 CrossRef
  3. Berner, RA, Morse, JW (1974) Dissolution kinetics of calcium carbonate in sea water IV. Theory of calcite dissolution. Am J Sci 274: pp. 134
  4. Borowitzka, MA, Larkum, AWD (1976) Calcification in the Green Alga Halimeda II. The exchange of Ca2+ and the occurence of age gradients in calcification and photosynthesis. J Exp Bot 27: pp. 864-878 CrossRef
  5. Borowitzka, MA, Larkum, AWD (1976) Calcification in the Green Alga Halimeda III. The sources of inorganic carbon for photosynthesis and calcification and a model of the mechanism of calcification. J Exp Bot 27: pp. 879-893 CrossRef
  6. Borowitzka, MA, Larkum, AWD (1976) Calcification in the Green Alga Halimeda IV. The action of metabolis inhibitiors on photosynthesis and calcification. J Exp Bot 27: pp. 894-907 CrossRef
  7. Borowitzka, MA, Larkum, AWD (1977) Calcification in the green alga Halimeda. I. An ultrastructure study of thallus development. J Phycol 13: pp. 6-16
  8. Borowitzka, MA, Larkum, AWD (1987) Calcification in algae: mechanisms and the role of metabolism. Crit Rev Plant Sci 6: pp. 1-45 CrossRef
  9. Carpenter RC (1986) Partitioning herbivory and its effects on coral reef algal communities. Ecol Monogr 56:345鈥?63
  10. Chauvin, A, Denis, V, Cuet, P (2011) Is the response of coral calcification to seawater acidification related to nutrient loading?. Coral Reefs 30: pp. 911-923 CrossRef
  11. Comeau, S, Edmunds, PJ, Spindel, NB, Carpenter, RC (2013) The responses of eight coral reef calcifiers to increasing partial pressure of CO2 do not exhibit a tipping point. Limnol Oceanogr 58: pp. 388-398 CrossRef
  12. Davies, PS (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar Biol 101: pp. 389-395 CrossRef
  13. Delgado, O, Lapointe, BE (1994) Nutrient-limited productivity of calcareous versus fleshy macroalgae in a eutrophic, carbonate-rich tropical marine environment. Coral Reefs 13: pp. 151-159 CrossRef
  14. Haan, J, Visser, PM, Ganase, AE, Gooren, EE, Stal, LJ, Duyl, FC, Vermeij, MJA, Huisman, J (2014) Nitrogen fixation rates in algal turf communities of a degraded versus less degraded coral reef. Coral Reefs 33: pp. 1003-1015 CrossRef
  15. Diaz-Pulido G, McCook LJ, Larkum AWD, Hoegh-Guldberg O (2007) Vulnerability of macroalgae of the Great Barrier Reef to climate change. In: Johnson JE, Marshall PA (eds) Climate change and the great barrier reef: a vulnerability assessment. Great Barrier Reef Marine Park Authority, Townsville, pp 153鈥?92
  16. Dickson, AG (1990) Thermodynamics of the dissociation of boric acid in synthetic seawater from 273.15 to 318.15聽K. Deep-Sea Res Part A 37: pp. 755-766 CrossRef
  17. Dickson, A The carbon dioxide system in seawater: equilibrium chemistry and measurements. In: Riebesell, U, Fabry, VJ, Hansson, L, Gattuso, J-P eds. (2010) Guide to best practices for ocean acidification research and data reporting. Publications Office of the European Union, Luxembourgpp. 260
  18. Dickson, AG, Millero, FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res Part A 34: pp. 1733-1743 CrossRef
  19. Drew, EA (1983) Halimeda biomass, growth rates and sediment generation on reefs in the central Great Barrier Reef province. Coral Reefs 2: pp. 101-110 CrossRef
  20. Drew, EA, Abel, KM (1987) Studies on Halimeda II. Reproduction, particularly the seasonality of gametangia formation, in a number of species from the Great Barrier Reef Province. Coral Reefs 6: pp. 207-218 CrossRef
  21. Eilers, PHC, Peeters, JCH (1988) A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol Model 42: pp. 199-215 CrossRef
  22. Fabricius, KE, Langdon, C, Uthicke, S, Humphrey, C, Noonan, S, Death, G, Okazaki, R, Muehllehner, N, Glas, MS, Lough, JM (2011) Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat Clim Change 1: pp. 165-169 CrossRef
  23. Falkenberg, LJ, Russell, BD, Connell, SD (2012) Stability of strong species interactions resist the synergistic effects of local and global pollution in Kelp forests. PloS ONE.
  24. Falkenberg, LJ, Russell, BD, Connell, SD (2013) Contrasting resource limitations of marine primary producers: implications for competitive interactions under enriched CO2 and nutrient regimes. Oecologia 172: pp. 575-583 CrossRef
  25. Figueroa, FL, Escassi, L, P茅rez-Rodr铆guez, E, Korbee, N, Delia Giles, A, Johnsen, G (2003) Effects of short-term irradiation on photo inhibition and accumulation of mycosporine-like amino acids in sun and shade species of the red algal genus Porphyra. J Photochem Photobiol B 69: pp. 21-30 CrossRef
  26. Findlay, HS, Wood, HL, Kendall, MA, Spicer, JI, Twitchett, RJ, Widdicombe, S (2011) Comparing the impact of high CO2 on calcium carbonate structures in different marine organisms. Mar Biol Res 7: pp. 565-575 CrossRef
  27. Fischer, JP, Koop-Jakobsen, K (2012) The multi fiber optode (MuFO): a novel system for simultaneous analysis of multiple fiber optic oxygen sensors. Sens Actuators B 168: pp. 354-359 CrossRef
  28. Froelich AS (1983). Functional aspects of nutrient cycling on coral reefs. In: Reaka ML (ed) 鈥楾he Ecology of Deep and Shallow Coral Reefs, Symposia Series for Undersea Research鈥欌€? vol 1. NOAA, National Undersea Research Program, Rockville, pp. 133鈥?39
  29. Frost-Christensen, H, Sand-Jensen, K (1992) The quantum efficiency of photosynthesis in macroalgae and submerged angiosperms. Oecologia 91: pp. 377-384 CrossRef
  30. Gao, K, Zheng, Y (2010) Combined effects of ocean acidification and solar UV radiation on photosynthesis, growth, pigmentation and calcification of the coralline alga Corallina sessilis (Rhodophyta). Glob Change Biol 16: pp. 2388-2398 CrossRef
  31. Gao, K, Aruga, Y, Asada, K, Ishihara, T, Akano, T, Kiyohara, M (1991) Enhanced growth of the red alga Porphyra yezoensis Ueda in high CO2 concentrations. J Appl Phycol 3: pp. 355-362 CrossRef
  32. Gao, K, Aruga, Y, Asada, K, Kiyohara, M (1993) Influence of enhanced CO2 on growth and photosynthesis of the red algae Gracilaria sp. and G. chilensis. J Appl Phycol 5: pp. 563-571 CrossRef
  33. Gast GJ (1998) Nutrient pollution in coral reef waters. Reef Care Cura莽ao Contribution no. 5. http://www.nacri.org/greylit/GastNutrPollWorkshop.html. Accessed 8 Aug 2007
  34. Gordillo, FJ, Niell, FX, Figueroa, FL (2001) Non-photosynthetic enhancement of growth by high CO2 level in the nitrophilic seaweed Ulva rigida C. Agardh (Chlorophyta). Planta 213: pp. 64-70 CrossRef
  35. Grzymski, J, Johnsen, G, Sakshaug, E (1997) The significance of intracellular self-shading on the biooptical properties of brown, red, and green macroalgae. J Phycol 33: pp. 408-414 CrossRef
  36. Hay, ME, Kappel, QE, Fenical, W (1994) Synergisms in plant defenses against herbivores: interactions of chemistry, calcification, and plant quality. Ecology 75: pp. 1714-1726 CrossRef
  37. Hillis L (1997) Coralgal reefs from a calcareous green alga perspective, and a first carbonate budget. In: Proceedings of the 8th international coral reef symposium, Panama, pp 761鈥?66
  38. Hillis-Colinvaux, L (1980) Ecology and taxonomy of Halimeda: primary producer of Coral Reefs. Adv Mar Biol 17: pp. 1-327 CrossRef
  39. Hoegh-Guldberg, O, Mumby, PJ, Hooten, AJ, Steneck, RS, Greenfield, P, Gomez, E, Harvell, CD, Sale, PF, Edwards, AJ, Caldeira, K, Knowlton, N, Eakin, CM, Iglesias-Prieto, R, Muthiga, N, Bardbury, RH, Dubi, A, Hatziolos, ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318: pp. 1737-1742 CrossRef
  40. Hofmann, LC, Straub, S, Bischof, K (2012) Competition between calcifying and noncalcifying temperate marine macroalgae under elevated CO2 levels. Mar Ecol Prog Ser 464: pp. 89-105 CrossRef
  41. Hofmann, LC, Yildiz, G, Hanelt, D, Bischof, K (2012) Physiological responses of the calcifying rhodophyte Corallina officinalis (L.) to future CO2 levels. Mar Biol 159: pp. 783-792 CrossRef
  42. Holcomb, M, McCorkle, DC, Cohen, AL (2010) Long-term effects of nutrient and CO2 enrichment on the temperate coral Astrangia poculata (Ellis and Solander 1786). J Exp Mar Biol Ecol 386: pp. 27-33 CrossRef
  43. Hurd, CL, Cornwall, CE, Currie, K, Hepburn, CD, McGraw, CM, Hunter, KA, Boyd, PW (2011) Metabolically-induced pH fluctuations by some coastal calcifiers exceed projected 22nd century ocean acidification: a mechanism for differential susceptibility?. Glob Change Biol 17: pp. 3254-3262 CrossRef
  44. Johnson, MD, Price, NN, Smith, JE (2014) Contrasting effects of ocean acidification on fleshy and calcareous algae. Peer J 2: pp. E411 CrossRef
  45. Jokiel, PL, Rodgers, KS, Kuffner, IB, Andersson, AJ, Cox, EF, Mackenzie, FT (2008) Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27: pp. 473-483 CrossRef
  46. Koroleff, F Determination of phosphorus. In: Grasshoff, K, Ehrhardt, M, Kremling, F eds. (1983) Methods of seawater analysis. Chemie, Weinheim, pp. 125-139
  47. K眉bler, JE, Johnston, AM, Raven, JA (1999) The effects of reduced and elevated CO2 and O2 on the seaweed Lomentaria articulata. Plant Cell Environ 22: pp. 1303-1310 CrossRef
  48. Kuffner, IB, Andersson, AJ, Jokiel, PL, Rodgers, KS, Mackenzie, FT (2008) Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci 1: pp. 114-117 CrossRef
  49. Langer, G, Geisen, M, Baumann, KH, Kl盲s, J, Riebesell, U, Thoms, S, Young, JR (2006) Species-specific responses of calcifying algae to changing seawater carbonate chemistry. Geochem Geophys Geosystems 7: pp. 1-12 CrossRef
  50. Lapointe, BE, Littler, MM, Littler, DS (1987) A comparison of nutrient-limited productivity in macroalgae from a Caribbean barrier reef and from a mangrove ecosystem. Aquat Bot 28: pp. 243-255 CrossRef
  51. Lapointe BE, Littler MM, Littler DS (1997) Macroalgal overgrowth of fringing coral reefs at Discovery Bay, Jamaica: bottom-up versus top-down control. In: Proceedings of the 8th international coral reef symosium vol 1, Panama, pp 927鈥?23
  52. Littler, MM, Littler, DS, Lapointe, BE (1988) A comparison of nutrient-and light-limited photosynthesis in psammophytic versus epilithic forms of Halimeda (Caulerpales, Halimedaceae) from the Bahamas. Coral Reefs 6: pp. 219-225 CrossRef
  53. Littler, MM, Littler, DS, Brooks, BL (2006) Harmful algae on tropical coral reefs: bottom-up eutrophication and top-down herbivory. Harmful Algae 5: pp. 565-585 CrossRef
  54. Marshall, JF, Davies, PJ (1988) Halimeda bioherms of the northern Great Barrier Reef. Coral Reefs 6: pp. 139-148 CrossRef
  55. Martin, S, Gattuso, JP (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Change Biol 15: pp. 2089-2100 CrossRef
  56. Matthiessen, B, Eggers, SL, Krug, S (2012) High nitrate to phosphorus regime attenuates negative effects of rising pCO2 on total population carbon accumulation. Biogeosciences 9: pp. 1195-1203 CrossRef
  57. Mattson, WJ, Julkunen-Tiitto, R, Herms, DA (2005) CO2 enrichment and carbon partitioning to phenolics: do plant responses accord better with the protein competition or the growth differentiation balance models?. Oikos 111: pp. 337-347 CrossRef
  58. McConnaughey, TA, Whelan, JF (1997) Calcification generates protons for nutrient and bicarbonate uptake. Earth Sci Rev 42: pp. 95-117 CrossRef
  59. McManus, JW, Polsenberg, JF (2004) Coral-algal phase shifts on coral reefs: ecological and environmental aspects. Prog Oceanogr 60: pp. 263-279 CrossRef
  60. Mehrbach, C, Culberson, CH, Hawley, JE, Pytkowicz, RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18: pp. 897-907 CrossRef
  61. Milliman, JD (1993) Production and accumulation of calcium carbonate in the ocean: budget of a nonsteady state. Glob Biogeochem Cycles 7: pp. 927-957 CrossRef
  62. Mwashote, BM, Jumba, IO (2002) Quantitative aspects of inorganic nutrient fluxes in the Gazi Bay (Kenya): implications for coastal ecosystems. Mar Pollut Bull 44: pp. 1194-1205 CrossRef
  63. Porzio, L, Buia, MC, Hall-Spencer, JM (2011) Effects of ocean acidification on macroalgal communities. J Exp Mar Biol Ecol 400: pp. 278-287 CrossRef
  64. Price, NN, Hamilton, SL, Smith, JE (2011) Species-specific consequences of ocean acidification for the calcareous tropical green algae Halimeda. Mar Ecol Prog Ser 440: pp. 67-78 CrossRef
  65. Rasheed, M, Badran, MI, Richter, C, Huettel, M (2002) Effect of reef framework and bottom sediment on nutrient enrichment in a coral reef of the Gulf of Aqaba, Red Sea. Mar Ecol Prog Ser 239: pp. 277-285 CrossRef
  66. Rees, SA, Opdyke, BN, Wilson, PA, Henstock, TJ (2007) Significance of Halimeda bioherms to the global carbonate budget based on a geological sediment budget for the Northern Great Barrier Reef, Australia. Coral Reefs 26: pp. 177-188 CrossRef
  67. Renegar, DA, Riegl, BM (2005) Effect of nutrient enrichment and elevated CO2 partial pressure on growth rate of Atlantic scleractinian coral Acropora cervicornis. Mar Ecol Prog Ser 293: pp. 69-76 CrossRef
  68. Ries, JB (2009) Effects of secular variation in seawater Mg/Ca ratio (calcite-aragonite seas) on CaCO3 sediment production by the calcareous algae Halimeda, Penicillus and Udotea-evidence from recent experiments and the geological record. Terra Nova 21: pp. 323-339 CrossRef
  69. Ries, JB, Cohen, AL, McCorkle, DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37: pp. 1131 CrossRef
  70. Robbins, LL, Knorr, PO, Hallock, P (2009) Response of Halimeda to ocean acidification: field and laboratory evidence. Biogeosci Discuss 6: pp. 4895-4918 CrossRef
  71. Roth盲usler, E, G贸mez, I, Karsten, U, Tala, F, Thiel, M (2011) UV-radiation versus grazing pressure: long-term floating of kelp rafts (Macrocystis pyrifera) is facilitated by efficient photo acclimation but undermined by grazing losses. Mar Biol 158: pp. 127-141 CrossRef
  72. Russell, BD, Thompson, J-A, 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: pp. 2153-2162 CrossRef
  73. Sinutok, S, Hill, R, Doblin, MA, Wuhrer, R, Ralph, PJ (2011) Warmer more acidic conditions cause decreased productivity and calcification in subtropical coral reef sediment-dwelling calcifiers. Limnol Oceanogr 56: pp. 1200-1212 CrossRef
  74. Stachowicz, JJ, Hay, ME (1999) Reducing predation through chemically mediated camouflage: indirect effects of plant defenses on herbivores. Ecology 80: pp. 495-509 CrossRef
  75. Steinberg, PD (1984) Algal chemical defense against herbivores: allocation of phenolic compounds in the kelp Alaria marginata. Science 223: pp. 405-407 CrossRef
  76. Steinberg, PD (1986) Chemical defenses and the susceptibility of tropical marine brown algae to herbivores. Oecologia 69: pp. 628-630 CrossRef
  77. Su谩rez-脕lvarez, S, G贸mez-Pinchetti, JL, Garc铆a-Reina, G (2012) Effects of increased CO2 levels on growth, photosynthesis, ammonium uptake and cell composition in the macroalga Hypnea spinella (Gigartinales, Rhodophyta). J Appl Phycol 24: pp. 815-823 CrossRef
  78. Targett, NM, Arnold, TM (1998) Minireview鈥攑redicting the effects of brown algal phlorotannins on marine herbivores in tropical and temperate oceans. J Phycol 34: pp. 195-205 CrossRef
  79. Targett, NM, Coen, LD, Boettcher, AA, Tanner, CE (1992) Biogeographic comparisons of marine algal polyphenolics: evidence against a latitudinal trend. Oecologia 89: pp. 464-470 CrossRef
  80. Teichberg, M, Fricke, A, Bischof, K (2013) Increased physiological performance of the calcifying green macroalga Halimeda opuntia in response to experimental nutrient enrichment on a Caribbean coral reef. Aquat Bot 104: pp. 25-33 CrossRef
  81. Thacker, R, Ginsburg, D, Paul, V (2001) Effects of herbivore exclusion and nutrient enrichment on coral reef macroalgae and cyanobacteria. Coral Reefs 19: pp. 318-329 CrossRef
  82. Webb, KL, DuPaul, WD, Wiebe, W, Sottile, W, Johannes, RE (1975) Enewetak (Eniwetok) Atoll: aspects of the nitrogen cycle on a coral reef. Limnol Oceanogr 20: pp. 198-210 CrossRef
  83. Wiebe, WJ, Johannes, RE, Webb, KL (1975) Nitrogen fixation in a coral reef community. Science 188: pp. 257-259 CrossRef
  84. Zabala, M, Ballesteros, E (1989) Surface-dependent strategies and energy flux in benthic marine communities or, why corals do not exist in the Mediterranean. Sci Mar 53: pp. 3-17
  85. Zou, D (2005) Effects of elevated atmospheric CO2 on growth, photosynthesis and nitrogen metabolism in the economic brown seaweed, Hizikia fusiforme (Sargassaceae, Phaeophyta). Aquaculture 250: pp. 726-735 CrossRef
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Ecology
  Plant Sciences
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-1939

文摘

Ocean acidification studies in the past decade have greatly improved our knowledge of how calcifying organisms respond to increased surface ocean CO2 levels. It has become evident that, for many organisms, nutrient availability is an important factor that influences their physiological responses and competitive interactions with other species. Therefore, we tested how simulated ocean acidification and eutrophication (nitrate and phosphate enrichment) interact to affect the physiology and ecology of a calcifying chlorophyte macroalga (Halimeda opuntia (L.) J.V. Lamouroux) and its common noncalcifying epiphyte (Dictyota sp.) in a 4-week fully crossed multifactorial experiment. Inorganic nutrient enrichment (+NP) had a strong influence on all responses measured with the exception of net calcification. Elevated CO2 alone significantly decreased electron transport rates of the photosynthetic apparatus and resulted in phosphorus limitation in both species, but had no effect on oxygen production or respiration. The combination of CO2 and +NP significantly increased electron transport rates in both species. While +NP alone stimulated H. opuntia growth rates, Dictyota growth was significantly stimulated by nutrient enrichment only at elevated CO2, which led to the highest biomass ratios of Dictyota to Halimeda. Our results suggest that inorganic nutrient enrichment alone stimulates several aspects of H. opuntia physiology, but nutrient enrichment at a CO2 concentration predicted for the end of the century benefits Dictyota sp. and hinders its calcifying basibiont H. opuntia.