, Volume 239, Issue 1, pp 231–242 | Cite as

Nutrient availability affects the response of the calcifying chlorophyte Halimeda opuntia (L.) J.V. Lamouroux to low pH

  • Laurie C. Hofmann
  • Jasmin Heiden
  • Kai Bischof
  • Mirta Teichberg
Original Article


Atmospheric carbon dioxide emissions cause a decrease in the pH and aragonite saturation state of surface ocean water. As a result, calcifying organisms are expected to suffer under future ocean conditions, but their physiological responses may depend on their nutrient status. Because many coral reefs experience high inorganic nutrient loads or seasonal changes in nutrient availability, reef organisms in localized areas will have to cope with elevated carbon dioxide and changes in inorganic nutrients. Halimeda opuntia is a dominant calcifying primary producer on coral reefs that contributes to coral reef accretion. Therefore, we investigated the carbon and nutrient balance of H. opuntia exposed to elevated carbon dioxide and inorganic nutrients. We measured tissue nitrogen, phosphorus and carbon content as well as the activity of enzymes involved in inorganic carbon uptake and nitrogen assimilation (external carbonic anhydrase and nitrate reductase, respectively). Inorganic carbon content was lower in algae exposed to high CO2, but calcification rates were not significantly affected by CO2 or inorganic nutrients. Organic carbon was positively correlated to external carbonic anhydrase activity, while inorganic carbon showed the opposite correlation. Carbon dioxide had a significant effect on tissue nitrogen and organic carbon content, while inorganic nutrients affected tissue phosphorus and N:P ratios. Nitrate reductase activity was highest in algae grown under elevated CO2 and inorganic nutrient conditions and lowest when phosphate was limiting. In general, we found that enzymatic responses were strongly influenced by nutrient availability, indicating its important role in dictating the local responses of the calcifying primary producer H. opuntia to ocean acidification.


Nitrate reductase Carbonic anhydrase Calcification Ocean acidification Eutrophication Photosynthesis 



The authors would like to thank Christian Brandt and Andrian Basilico for help with the experimental set-up, Dorothea Dasbach for tissue carbon and nitrogen analysis and Matthias Birkicht for dissolved inorganic nutrient analysis. Funding for this project was provided by the German Federal Ministry of Education and Research (BMBF) through the cooperative research project Biological Impacts of Ocean Acidification (BIOACID).


  1. Albright R, Mason B, Langdon C (2008) Effect of aragonite saturation state on settlement and post-settlement growth of Porites astreoides larvae. Coral Reefs 27:485–490CrossRefGoogle Scholar
  2. Albright R, Mason B, Miller M, Langdon C (2010) Ocean acidification compromises recruitment success of the threatened Caribbean coral Acropora palmata. Proc Natl Acad Sci USA. doi: 107:20400-20404 PubMedGoogle Scholar
  3. Alexandre A, Silva J, Buapet P, Björk M, Santos R (2012) Effects of CO2 enrichment on photosynthesis, growth, and nitrogen metabolism of the seagrass Zostera noltii. Ecol Evol 2:2625–2635PubMedCentralPubMedCrossRefGoogle Scholar
  4. Andersson AJ, Kuffner IB, Mackenzie FT, Jokiel PL, Rodgers KS, Tan A (2009) Net loss of CaCO3 from coral reef communities due to human induced seawater acidification. Biogeosci Discuss 6:2163–2182CrossRefGoogle Scholar
  5. Andria J, Vergara J, Perez-Llorens JL (1999) Biochemical responses and photosynthetic performance of Gracilaria sp. (Rhodophyta) from Cádiz, Spain, cultured under different inorganic carbon and nitrogen levels. Eur J Phycol 34:497–504CrossRefGoogle Scholar
  6. Borowitzka MA, Larkum AWD (1976) Calcification in the Green Alga Halimeda III. The sorces of inorganic carbon for photosynthesis and calcification and a model of the mechanism of calcification. J Exp Bot 27:879–889CrossRefGoogle Scholar
  7. Brewer PG (1997) Ocean chemistry of the fossil fuel CO2 signal: the haline signal of “business as usual”. Geophys Res Lett 24(11):1367–1369CrossRefGoogle Scholar
  8. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365PubMedCrossRefGoogle Scholar
  9. Chauvin A, Denis V, Cuet P (2011) Is the response of coral calcification to seawater acidification related to nutrient loading? Coral Reefs 30:911–923CrossRefGoogle Scholar
  10. Corzo A, Niell FX (1991) Determination of nitrate reductase activity in Ulva rigida C. Agardh by the in situ method. J Exp Mar Biol Ecol 146:181–191CrossRefGoogle Scholar
  11. Delgado O, Lapointe BE (1994) Nutrient-limited productivity of calcareous versus fleshy macroalgae in a eutrophic, carbonate-rich tropical marine environment. Coral Reefs 13:151–159CrossRefGoogle Scholar
  12. Demes KW, Bell SS, Dawes CJ (2009) The effects of phosphate on the biomineralization of the green alga, Halimeda incrassata (Ellis) Lam. J Exp Mar Biol Ecol 374:123–127CrossRefGoogle Scholar
  13. Demes KW, Littler MM, Littler DS (2010) Comparative phosphate acquisition in giant-celled rhizophytic algae (Bryopsidales, Chlorophyta): fleshy vs. calcified forms. Aquat Bot 92:157–160CrossRefGoogle Scholar
  14. Diaz-Pulido G, McCook LJ, Larkum AWD, Lotze HK, Raven JA, Schaffelke B, Smith JS, Steneck RS (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 and Australian Greenhouse Office, AustraliaGoogle Scholar
  15. Dickson, AG (1990) Thermodynamics of the dissociation of boric acid in synthetic seawater from 273.15 to 318.15 K: deep sea research Part A. Oceanogr Res Papers 37(5):755–766Google Scholar
  16. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep sea research Part A. Oceanogr Res Papers 34:1733–1743Google Scholar
  17. Drew EA (1983) Halimeda biomass, growth rates and sediment generation on reefs in the central Great Barrier Reef province. Coral Reefs 2:101–110CrossRefGoogle Scholar
  18. Drew EA, Abel KM (1988) Studes on Halimeda II. Reproduction, particularly the seasonality of gametangia formation, in a number of species from the Great Barrier Reef Province. Coral Reefs 6:207–218CrossRefGoogle Scholar
  19. Eilers PHC, Peeters JCH (1988) A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol Model 42:199–215CrossRefGoogle Scholar
  20. Fabricius KE (2005) Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar Pollut Bull 50:125–146PubMedCrossRefGoogle Scholar
  21. Fabricius KE, Langdon C, Uthicke S, Humphrey C, Noonan S, De’ath 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 1:165–169CrossRefGoogle Scholar
  22. Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414CrossRefGoogle Scholar
  23. Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ, Millero FJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366PubMedCrossRefGoogle Scholar
  24. 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 7:565–575CrossRefGoogle Scholar
  25. Fong P, Boyer KE, Kamer K, Boyle KA (2003) Influence of initial tissue nutrient status of tropical marine algae on response to nitrogen and phosphorus additions. Mar Ecol Prog Ser 262:111–123CrossRefGoogle Scholar
  26. Fricke A, Teichberg M, Beilfuss S, Bischof K (2011) Succession patterns in algal turf vegetation on a Caribbean coral reef. Bot Mar 54:111–125CrossRefGoogle Scholar
  27. 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 Chang Biol 16:2388–2398CrossRefGoogle Scholar
  28. Gao K, Juntian Xu, Guang Gao, Li Yahe, Hutchins DA, Huang B, Wang L, Zheng Y, Jin P, Cai X, Häder D-P, Li W, Xu K, Liu N, Ribesell U (2012) Rising CO2 and increased light exposure syngergistically reduce marine primary productivity. Nat Clim Chang 2:519–523Google Scholar
  29. Geiger M, Haake V, Ludewig F, Sonnewald U, Stitt M (1999) The nitrate and ammonium nitrate supply have a major influence on the response of photosynthesis, carbon metabolism, nitrogen metabolism and growth to elevated carbon dioxide in tobacco. Plant Cell Environ 22:1177–1199CrossRefGoogle Scholar
  30. 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 213:64–70PubMedCrossRefGoogle Scholar
  31. Gordillo FJ, Aguilera J, Jiménez C (2006) The response of nutrient assimilation and biochemical composition of Arctic seaweeds to a nutrient input in summer. J Exp Bot 57:2661–2671PubMedCrossRefGoogle Scholar
  32. Guinotte JM, Fabry VJ (2008) Ocean acidification and its potential effects on marine ecosystems. Ann N Y Acad Sci 1134:320–342PubMedCrossRefGoogle Scholar
  33. Guinotte JM, Buddemeier RW, Kleypas JA (2003) Future coral reef habitat marginality: temporal and spatial effects of climate change in the Pacific basin. Coral Reefs 22:551–558CrossRefGoogle Scholar
  34. Haglund K, Björk M, Rmazanov Z, García-Reina G, Pedersén M (1992) Role of carbonic anhydrase in photosynthesis and inorganic–carbon assimilation in the red alga Gracilaria tenuistipitata. Planta 187:275–281PubMedCrossRefGoogle Scholar
  35. Hillis L (1997) Coralgal reefs from a calcareous green alga perspective, and a first carbonate budget. Proc 8th Int Coral Reef Symp Panama 1:761–766Google Scholar
  36. Hillis-Colinvaux L (1980) Ecology and taxonomy of Halimeda: primary producer of coral reefs. Adv Mar Biol 17:1–327Google Scholar
  37. Hocking PJ, Meyer CP (1991) Effects of CO2 enrichment and nitrogen stress on growth, and partitioning of dry matter and nitrogen in wheat and maize. Funct Plant Biol 18:339–356Google Scholar
  38. 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, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742PubMedCrossRefGoogle Scholar
  39. Hofmann LC, Bischof K, Baggini C, Koop-Jakobsen K, Johnson A, Teichberg M (2013a) CO2 and inorganic nutrient enrichment affect the performance and competitive strength of a calcifying green alga and its noncalcifying epiphyte. Oecologia (submitted)Google Scholar
  40. Hofmann LC, Straub S, Bischof K (2013b) Elevated CO2 levels affect the activity of nitrate reductase and carbonic anhydrase in the calcifying rhodophyte Corallina officinalis. J Exp Bot 64:899–908PubMedCrossRefGoogle Scholar
  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 159:783–792CrossRefGoogle Scholar
  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 386:27–33CrossRefGoogle Scholar
  43. Huppe HC, Turpin DH (1994) Integration of carbon and nitrogen metabolism in plant and algal cells. Annu Rev Plant Biol 45:577–607Google Scholar
  44. 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 45:1236–1251CrossRefGoogle Scholar
  45. Jan Gast G (1998) Nutrient pollution in coral reef waters. Syllabus for the reef care Curacao workshop on nutrient pollution. Reef care Curacao Contribution no. 5. (Accessed 18 June 2013)
  46. Johnson VR, Brownlee C, Rickaby REM, Graziano M, Milazzo M, Hall-Spencer JM (2011) Responses of marine benthic microalgae to elevated CO2. Mar Biol 160:1813–1824CrossRefGoogle Scholar
  47. Jokiel PL, Rodgers KS, Kuffner IB, Andersson AJ, Cox EF, Mackenzie FT (2008) Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27:473–483CrossRefGoogle Scholar
  48. Kleypas JA, Feely RA, Fabry VJ, Langdon C, Sabine CL, Robbins LL (2006) Impacts of ocean acidification on coral reefs and other marine calcifiers: a guide for future research, report of a workshop held 18–20 April 2005. St. Petersburg, FL, sponsored by NSF, NOAA, and the US Geological SurveyGoogle Scholar
  49. Koroleff F (1983) Determination of phosphorus. In: Grasshoff K, Ehrhardt M, Kremling F (eds) Methods of seawater analysis. Verlag chemie, Weinheim, pp 125–139Google Scholar
  50. Kuenen M, Debrot AO (1995) A quantitative study of the seagrass and algal meadows of the spaanse water, Curaçao, The Netherlands Antilles. Aquat Bot 51:291–331CrossRefGoogle Scholar
  51. Langdon C, Takahashi T, Chipman D, Goddard J (2000) Effect of calcium carbonate saturation state on the calcification rate of an experimental reef. Glob Biogeochem Cycles 14:639–654CrossRefGoogle Scholar
  52. Langdon C, Broecker WS, Hammond DE, Glenn E, Fitzsimmons K, Nelson SG, Peng TH, Hajdas I, Bonani G (2003) Effect of elevated CO2 on the community metabolism of an experimental coral reef. Glob Biogeochem Cycles 17:1–14CrossRefGoogle Scholar
  53. Lapointe BE (1987) Phosphorus- and nitrogen-limited photosynthesis and growth of Gracilaria tikbahiae (Rhodophyceae) in the Florida Keys: an experimental field study. Mar Biol 93:561–568CrossRefGoogle Scholar
  54. Leclercq NI, Gattuso JP, Jaubert J (2000) CO2 partial pressure controls the calcification rate of a coral community. Glob Chang Biol 6:329–334CrossRefGoogle Scholar
  55. 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 6:219–225CrossRefGoogle Scholar
  56. Liu Y, Xu J, Gao K (2012) CO2-driven seawater acidification increases photochemical stress in a green alga. Phycologia 51:562–566CrossRefGoogle Scholar
  57. Losada M, Guerrero MG (1979) The photosynthetic reduction of nitrate and its regulation. Photosynthesis in relation to model systems. Elsevier, Amsterdam, pp 365–408Google Scholar
  58. Manzello DP (2010) Coral growth with thermal stress and ocean acidification: lessons from the eastern tropical Pacific. Coral Reefs 29:749–758CrossRefGoogle Scholar
  59. Marshall JF, Davies PJ (1988) Halimeda bioherms of the northern Great Barrier Reef. Coral Reefs 6:139–148CrossRefGoogle Scholar
  60. Matthiessen B, Eggers SL, Krug S (2012) High nitrate to phosphorus regime attenuates negative effects of rising pCO2 on total population carbon accumulation. Biogeosciences 9:1195–1203CrossRefGoogle Scholar
  61. McCook LJ (1999) Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18:357–367CrossRefGoogle Scholar
  62. McCulloch M, Falter J, Trotter J, Montagna P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Chang 2(7):1–5CrossRefGoogle Scholar
  63. 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 18:897–907CrossRefGoogle Scholar
  64. Milliman JD (1993) Production and accumulation of calcium carbonate in the ocean: budget of a nonsteady state. Glob Biogeochem Cycles 7:927–957CrossRefGoogle Scholar
  65. Nelson WA (2009) Calcified macroalgae-critical to coastal ecosystems and vulnerable to change: a review. Mar Freshw Res 60:787–801CrossRefGoogle Scholar
  66. Nicholas DJD, Scawin JH (1956) A phosphate requirement for nitrate reductase from Neurospora crassa. Nature 178:1474–1475CrossRefGoogle Scholar
  67. 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 437:681–686PubMedCrossRefGoogle Scholar
  68. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta–Bioenergetics 975:384–394CrossRefGoogle Scholar
  69. Price NN, Hamilton SL, Smith JE (2011) Species-specific consequences of ocean acidification for the calcareous tropical green algae Halimeda. Mar Ecol Prog Ser 440:67–78CrossRefGoogle Scholar
  70. Purvis AC, Peters DB, Hageman RH (1974) Effect of carbon dioxide on nitrate accumulation and nitrate reductase induction in corn seedlings. Plant Physiol 53:934–941PubMedCentralPubMedCrossRefGoogle Scholar
  71. 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 26:177–188CrossRefGoogle Scholar
  72. 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 293:69–76CrossRefGoogle Scholar
  73. Reynaud S, Leclercq N, Romaine-Lioud S, Ferrier-Pages C, Jaubert J, Gattuso JP (2003) Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Glob Chang Biol 9:1660–1668CrossRefGoogle Scholar
  74. Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131CrossRefGoogle Scholar
  75. Robbins LL, Knorr PO, Hallock P (2009) Response of Halimeda to ocean acidification: field and laboratory evidence. Biogeosci Discuss 6:4895–4918CrossRefGoogle Scholar
  76. Robbins, LL, Hansen, ME, Kleypas, JA, and Meylan, SC (2010) CO2calc—a user-friendly seawater carbon calculator for Windows, Max OS X, and iOS (iPhone). U.S. Geological Survey Open-File Report 2010–1280Google Scholar
  77. Rokitta SD, John U, Rost B (2012) Ocean acidification affects redox-balance and ion-homeostasis in the life-cyce stages of Emiliania huxleyi. PLoS ONE 7:e52212. doi: 10.1371/journal.pone.0052212 PubMedCentralPubMedCrossRefGoogle Scholar
  78. 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 Chang Biol 15:2153–2162CrossRefGoogle Scholar
  79. Ryther JH, Dunstan WM (1971) Nitrogen, phosphorus, and eutrophication in the coastal marine environment. Science 171:1008PubMedCrossRefGoogle Scholar
  80. 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 56:1200CrossRefGoogle Scholar
  81. Smith SV (1984) Phosphorus versus nitrogen limitation in the marine environment. Limnol Oceanogr 29:1149–1160CrossRefGoogle Scholar
  82. Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 22:583–621CrossRefGoogle Scholar
  83. Syrett PJ (1981) Nitrogen metabolism of microalgae. Can Bull Fish Aquat Sci 210:182–210Google Scholar
  84. 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 104:25–33CrossRefGoogle Scholar
  85. Turpin DH (1991) Effects of inorganic N availability on algal photosynthesis and carbon metabolism. J Phycol 27:14–20CrossRefGoogle Scholar
  86. Turpin DH, Elrifi IR, Birch DG, Weger HG, Holmes JJ (1988) Interactions between photosynthesis, respiration, and nitrogen assimilation in microalgae. Can J Bot 66:2083–2097Google Scholar
  87. van den Hoek C, Colijn F, Cortel-Breeman AM, Wanders JB (1972) Algal vegetation types along the shores of inner bays and lagoons of curacao and the lagoon Lac (Bonaire), Netherlands Antilles. Elsevier, HollandGoogle Scholar
  88. van den Hoek C, Cortel-Breeman AM, Wanders JBW (1975) Algal zonation in the fringing coral reef of Curacao, Netherlands Antilles, in relation to zonation of corals and gorgonians. Aquat Bot 1:269–308CrossRefGoogle Scholar
  89. Wu Y, Gao K, Riebesell U (2010) CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences Discuss 7:3855–3878CrossRefGoogle Scholar
  90. Xia JR, Gao KS (2005) Impacts of elevated CO2 concentration on biochemical composition, carbonic anhydrase, and nitrate reductase activity of freshwater green algae. J Integr Plant Biol 47:668–675CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Laurie C. Hofmann
    • 1
  • Jasmin Heiden
    • 2
  • Kai Bischof
    • 1
  • Mirta Teichberg
    • 2
  1. 1.Marine Botany Department, Bremen Marine Ecology Center for Research and EducationUniversity of BremenBremenGermany
  2. 2.Leibniz Center for Tropical Marine EcologyBremenGermany

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