Experimental assessment of organic carbon fluxes in the scleractinian coral Stylophora pistillata during a thermal and photo stress event

Marine Ecology Progress Series

Volumn 453, Issue , 2012, Pages 63-77

  Tremblay, Pascale ^a   Naumann, Malik S ^a,b   Sikorski, Séverine ^a   Grover, Renaud ^a   Ferrier Pagès, Christine ^a  

^a CENTRE SCIENTIFIQUE DE MONACO   (Monaco)

^b UNIVERSITY OF BREMEN   (Germany)

Author keywords

Coral bleaching; Dissolved free amino acids; Light stress; Nanoplankton; Picoplankton; Temperature stress; Total organic carbon

Indexed keywords

AMINO ACID; AUTOTROPHY; CARBON FLUX; CORAL; CORAL BLEACHING; ENDANGERED SPECIES; GRAZING; HETEROTROPHY; LIGHT EFFECT; NANOPLANKTON; NUTRIENT UPTAKE; PICOPLANKTON; RESPIRATION; SYMBIONT; TEMPERATURE EFFECT; TOTAL ORGANIC CARBON;

ANTHOZOA; SCLERACTINIA; STYLOPHORA PISTILLATA;

EID: 84861037977     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps09640     Document Type: Article

References (91)

1. Al-Moghrabi S, Allemand D, Jaubert J (1993) Valine uptake by the scleractinian coral Galaxea fascicularis: character-ization and effect of light and nutritional status. J Comp Physiol B 163: 355-362
2. Anthony KRN, Fabricius KE (2000) Shifting roles of hetero -trophy and autotrophy in coral energy budgets at vari-able turbidity. J Exp Mar Biol Ecol 252: 221-253
3. Anthony KRN, Hoogenboom MO, Maynard JA, Grottoli AG, Middlebrook R (2009) Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct Ecol 23: 539-550
4. Bak RPM, Joenje M, de Jong I, Lambrechts DYM, Nieuw-land G (1998) Bacterial suspension feeding by coral reef benthic organisms. Mar Ecol Prog Ser 175: 285-288 (Pubitemid 29032666)
5. Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Coral reefs: corals' adaptive response to climate change. Nature 430: 741
6. Berkelmans R, van Oppen MJH (2006) The role of zooxan-thellae in the thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era of climate change. Proc Biol Sci 273: 2305-2312 (Pubitemid 44387337)
7. Borell EM, Yuliantri AR, Bischof K, Richter C (2008) The effect of heterotrophy on photosynthesis and tissue com-position of two scleractinian corals under elevated tem-perature. J Exp Mar Biol Ecol 364: 116-123
8. Bronk AD (2002) Dynamics of dissolved organic nitrogen. In: Hansell DA, Carison CA (eds) Biogeochemistry of marine dissolved organic matter. Academic Press, San Diego, CA, p 153-247
9. Brown BE (1997) Coral bleaching: causes and consequences. Coral Reefs 16: S129-S138
10. Buddemeier RW, Kleypas JA, Aronson R (2004) Coral reefs and global climate change. Potential contributions of cli-mate change to stresses on coral reef ecosystems. Pew Center on Global Climate Change, Arlington, VA
11. Bythell JC (1988) A total nitrogen and carbon budget for the elkhorn coral Acropora palmata (Lamarck). Proc 6th Int Coral Reef Symp 2: 535-540
12. Coffroth MA (1984) Ingestion and incorporation of coral mucus aggregates by a gorgonian soft coral. Mar Ecol Prog Ser 17: 193-199
13. Cossins AR, Bowler K (1987) Temperature biology of animals. Chapman & Hall, New York, NY
14. Donner SD, Skirving WJ, Little CM, Oppenheimer M, Hoegh-Guldberg O (2005) Global assessment of coral bleaching and required rates of adaptation under climate change. Glob Change Biol 11: 2251-2265 (Pubitemid 43904657)
15. Douglas AE (2003) Coral bleaching: how and why? Mar Pollut Bull 46: 385-392
16. Drollet JH, Faucon M, Martin PMV (1995) Elevated sea-water temperature and solar UV-B flux associated with two successive coral mass bleaching events in Tahiti. Mar Freshw Res 46: 1153-1157 (Pubitemid 2620292)
17. Edge SE, Morgan MB, Gleason DF, Snell TW (2005) Devel-opment of a coral cDNA array to examine gene expres-sion profiles in Montastraea faveolata exposed to envi-ronmental stress. Mar Pollut Bull 51: 507-523 (Pubitemid 41618393)
18. Edmunds PJ (1994) Evidence that reef-wide patterns of coral bleaching may be the result of the distribution of bleach-ing-susceptible clones. Mar Biol 121: 137-142
19. Ferrier MD (1991) Net uptake of dissolved free amino acids by four scleractinian corals. Coral Reefs 10: 183-187
20. Ferrier-Pagès C, Gattuso JP (1998) Biomass, production and grazing rates of pico- and nanoplankton in coral reef waters (Miyako Island, Japan). Microb Ecol35: 46-57 (Pubitemid 28031177)
21. Ferrier-Pagès C, Gattuso JP, Cauwet G, Jaubert J, Allemand D (1998) Release of dissolved organic carbon and nitro-gen by the zooxanthellate coral Galaxea fascicularis. Mar Ecol Prog Ser 172: 265-274 (Pubitemid 28504234)
22. Ferrier-Pagès C, Schoelzke V, Jaubert J, Muscatine L, Hoegh-Guldberg O (2001) Response of a scleractinian coral, Stylophora pistillata, to iron and nitrate enrich-ment. J Exp Mar Biol Ecol 259: 249-261 (Pubitemid 32428580)
23. Ferrier-Pagès C, Rottier C, Béraud É, Levy O (2010) Experi-mental assessment of the feeding effort of three sclerac-tinian coral species during a thermal stress: effect on the rates of photosynthesis. J Exp Mar Biol Ecol 390: 118-124
24. Ferrier-Pagès C, Hoogenboom M, Houlbrèque F (2011) The role of plankton in coral trophodynamics. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Heidelberg, p 215-229
25. Fitt WK, Brown BE, Warner ME, Dunne RP (2001) Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 20: 51-65 (Pubitemid 32770401)
26. Fitt WK, Gates RD, Hoegh-Guldberg O, Bythell JC and others (2009) Response of two species of Indo-Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: the host does matter in deter-mining the tolerance of corals to bleaching. J Exp Mar Biol Ecol 373: 102-110
27. Frost BW (1972) Effects of size and concentration of food par-ticles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol Oceanogr 17: 805-815
28. Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Glob Change Biol 2: 495-509 (Pubitemid 126670990)
29. Green RH (1979) Sampling design and statistical methods for environmental biologists. Wiley Interscience, Chichester
30. Grottoli AG, Rodrigues LJ, Juarez C (2004) Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleach-ing event. Mar Biol145: 621-631 (Pubitemid 39275454)
31. Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440: 1186-1189
32. Grover R, Maguer JF, Reynaud-Vaganay S, Ferrier-Pagès C (2002) Uptake of ammonium by the scleractinian coral Stylophora pistillata: effect of feeding, light, and ammo-nium concentrations. Limnol Oceanogr 47: 782-790 (Pubitemid 34527284)
33. Grover R, Maguer JF, Allemand D, Ferrier-Pagès C (2003) Nitrate uptake in the scleractinian coral Stylophora pis-tillata. Limnol Oceanogr 48: 2266-2274 (Pubitemid 37538078)
34. Grover R, Maguer JF, Allemand D, Ferrier-Pagès C (2008) Uptake of dissolved free amino acids by the scleractinian coral Stylophora pistillata. J Exp Biol 211: 860-865 (Pubitemid 351580054)
35. Hedges JI (1992) Global biogeochemical cycles: progress and problems. Mar Chem 39: 67-93 (Pubitemid 23377943)
36. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Mar Freshw Res 50: 839-866 (Pubitemid 30018479)
37. Hoegh-Guldberg O (2011) Coral reef ecosystems and anthro pogenic climate change. Reg Environ Change 11(Suppl 1): 215-227
38. Hoegh-Guldberg O, Smith GJ (1989) The effect of sudden changes in temperature, irradiance and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata Esper and Seriatopora hystrixDana. J Exp Mar Biol Ecol 129: 279-303 (Pubitemid 20420450)
39. Hoegh-Guldberg O, Williamson J (1999) Availability of two forms of dissolved nitrogen to the coral Pocillopora dam-icornis and its symbiotic zooxanthellae. Mar Biol 133: 561-570 (Pubitemid 29186660)
40. Hoogenboom M, Béraud É, Ferrier-Pagès C (2010) Relation-ship between symbiont density and photosynthetic car-bon acquisition in the temperate coral Cladocora caespi-tosa. Coral Reefs 29: 21-29
41. Houlbrèque F, Tambutté TE, Richard C, Ferrier-Pagès C (2004) Importance of a micro-diet for scleractinian corals. Mar Ecol Prog Ser 282: 151-160 (Pubitemid 39661294)
42. Houlbrèque F, Delesalle B, Blanchot J, Montel Y, Ferrier-Pagès C (2006) Picoplankton removal by the coral reef community of La Prévoyante, Mayotte Island. Aquat Microb Ecol 44: 59-70 (Pubitemid 44400886)
43. Hughes TP, Baird AH, Bellwood DR, Card M and others (2003) Climate change, human impacts, and the re -silience of coral reefs. Science 301: 929-933 (Pubitemid 36994796)
44. Iglesias-Prieto R, Matta J, Robins WA, Trench RK (1992) Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci USA 89: 10302-10305
45. 2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167: 191-194
46. Kato M (1987) Mucus-sheet formation and discoloration in the reef-building coral, Porites cylindrica: effects of altered salinity and temperature. Galaxea 6: 1-16
47. Lehman JT (1976) The filter-feeder as an optimal forager, and the predicted shapes of feeding curves. Limnol Oceanogr 21: 501-516
48. Lesser MP, Farrell J (2004) Exposure to solar radiation increases damage to both host tissues and algal sym-bionts of corals during thermal stress. Coral Reefs 23: 367-377 (Pubitemid 39320598)
49. Levy O, Mizrahi L, Chadwick-Furman NE, Achituv Y (2001) Factors controlling the expansion behaviour of Favia favus (Cnidaria: Scleractinia). Effects of light, flow and planktonic prey. Biol Bull 200: 118-126 (Pubitemid 32391886)
50. Loya Y, Sakai K, Yamazata K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4: 122-131 (Pubitemid 32228508)
51. MacArthur RH, Pianka ER (1966) Optimal use of a patchy environment. Am Nat 100: 603-609
52. Marshall PA, Baird AH (2000) Bleaching of corals on the great barrier reef: differential susceptibilities among taxa. Coral Reefs 19: 155-163 (Pubitemid 30610813)
53. Mass T, Kline DI, Roopin M, Veal CJ, Cohen S, Iluz D, Levy O (2010) The spectral quality of light is a key driver of photosynthesis and photoadaptation in Stylophora pistil-lata colonies from different depths in the Red Sea. J Exp Biol 213: 4084-4091
54. McCloskey LR, Muscatine L (1984) Production and respira-tion in the Red Sea coral Stylophora pistillata as a func-tion of depth. Proc R Soc Lond B Biol Sci 222: 215-230
55. Morgan MB, Edge SE, Snell TW (2005) Profiling differential gene expression of corals along a transect of waters adja-cent to the Bermuda municipal dump. Mar Pollut Bull 51: 524-533 (Pubitemid 41618394)
56. Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26: 601-611
57. 13C of zooxanthellae and animal tissue versus depth. Mar Biol 100: 185-193
58. Naumann MS, Niggl W, Laforsch C, Glaser G, Wild C (2009) Coral surface area quantification-evaluation of estab- lished techniques by comparison with computer tomo - graphy. Coral Reefs 28: 109-117
59. Naumann MS, Haas A, Struck U, Mayr C, el-Zibdah M, Wild C (2010a) Organic matter release by the dominant herma typic corals of the Northern Red Sea. Coral Reefs 29: 649-660
60. Naumann MS, Mayr C, Struck U, Wild C (2010b) Coral mucus stable isotope composition and labeling \- experi- mental evidence for mucus uptake by epizoic acoelo- morph worms. Mar Biol 157: 2521-2531
61. Naumann MS, Orejas C, Wild C, Ferrier-Pagès C (2011) First evidence for zooplankton feeding sustaining key physiological processes in a scleractinian cold-water coral. J Exp Biol 214: 3570-3576
62. Niggl W, Glas M, Laforsch C, Mayr C, Wild C (2009) First evidence of coral bleaching stimulating organic matter release by reef corals. Proc 11th Int Coral Reef Symp 2: 905-911
63. Palenik B, Morel FMM (1990) Amino acid utilization by marine phytoplankton: a novel mechanism. Limnol Oceanogr 35: 260-269
64. Parsons TR, Maita Y, Lalli CM (1984) Determination of dis- solved free amino acids by fluorometric analysis. In: Par- sons TR, Maita Y, Ialli CM (eds) A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford, p 40-44
65. Picciano M, Ferrier-Pagès C (2007) Grazing of pico- and nanoplankton by the Mediterranean red coral Corallium rubrum. Mar Biol 150: 773-778
66. Piggot AM, Fouke BW, Sivaguru M, Sanford RA, Gaskins HR (2009) Change in zooxanthellae and mucocyte tissue den- sity as an adaptive response to environmental stress by the coral, Montastraea annularis. Mar Biol 156: 2379-2389
67. Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25: 943-948
68. Ribes M, Coma R, Gili JM (1998) Heterotrophic feeding by gorgonian corals with symbiotic zooxanthella. Limnol Oceanogr 43: 1170-1179 (Pubitemid 28523686)
69. Ribes M, Coma R, Gili JM (1999) Natural diet and grazing rate of the temperate sponge Dysidea avara (Desmo- spongiae, Dendroceratida) throughout an annual cycle. Mar Ecol Prog Ser 176: 179-190 (Pubitemid 29107456)
70. Ribes M, Coma R, Rossi S (2003) Natural feeding of the tem- perate asymbiotic octocoral-gorgonian Leptogorgia sarmentosa (Cnidaria: Octocorallia). Mar Ecol Prog Ser 254: 141-150 (Pubitemid 36738285)
71. Rodolfo-Metalpa R, Richard C, Allemand D, Bianchi CN, Morri C, Ferrier-Pagès C (2006) Response of zooxanthellae in symbiosis with the Mediterranean corals Cladocora caespitosa and Oculina patagonica to elevated tem- peratures. Mar Biol 150: 45-55 (Pubitemid 44451054)
72. Rodrigues LJ, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleach- ing. Limnol Oceanogr52: 1874-1882 (Pubitemid 47612115)
73. Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430: 742 (Pubitemid 39071338)
74. Salih A, Hoegh-Guldberg O, Cox G (1998) Bleaching responses of symbiotic dinoflagellates in corals: the effects of light and elevated temperature on their morphology and physiology. In: Greenwood JG, Hall NJ (eds) Proc Australian Coral Reef Soc 75th Anniversary Conf, University of Queenland, Brisbane, p 199-216
75. SheldonRW, RassoulzadeganF (1987) A method for measur-ing plankton production by particle counting. Mar Microb Food Webs 2: 29-44
76. Shick JM, Ferrier-Pagès C, Grover R, Allemand D (2005) Effects of starvation, ammonium concentration, and photo synthesis on the UV-dependent accumulation of mycosporine-like amino acids (MAAs) in the coral Sty-lophora pistillata. Mar Ecol Prog Ser 295: 135-156 (Pubitemid 41026818)
77. Smith EP (2002) BACI design. In: El-Shaarawi AH, Piegorsch WW (eds) Encyclopedia of environmetrics, Vol 1. John Wiley & Sons Ltd, Chichester, p 141-148
78. Smith PK, Khrohn RI, Hermanson GT, Malia AK and others (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85 (Pubitemid 16258399)
79. Sorokin Y (1991) Parameters of productivity and metabo-lisms on coral reef ecosystems off central Vietnam. Estuar Coast Shelf Sci 33: 259-280
80. Stewart-Oaten A, Murdoch WW, Parker KR (1986) Environ-mental impact assessment: 'pseudoreplication' in time? Ecology 67: 929-940
81. Stimson J, Kinzie RA (1991) The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen enrichment and control conditions. J Exp Mar Biol Ecol 153: 63-74
82. Stimson J, Sakai K, Sembali H (2002) Interspecific compari-son of the symbiotic relationship in corals with high and low rates of bleaching-induced mortality. Coral Reefs 21: 409-421 (Pubitemid 36064607)
83. Tolosa I, Treignier C, Grover R, Ferrier-Pagès C (2011) Impact of feeding and short-term temperature stress on the content and isotopic signature of fatty acids, sterols, and alcohols in the scleractinian coral Turbinaria reni-formis. Coral Reefs 30: 763-774
84. Treignier C, Grover R, Ferrier-Pagès C (2008) Effect of light and feeding on the fatty acid and sterol composition of zooxanthellae and host tissue isolated from the sclerac-tinian coral Turbinaria reniformis. Limnol Oceanogr 53: 2702-2710
85. Tremblay P, Peirano A, Ferrier-Pagès C (2011) Heterotrophy in the Mediterranean symbiotic coral Cladocora caespi-tosa: comparison with two other scleractinian species. Mar Ecol Prog Ser 422: 165-177
86. Underwood AJ (1994) On beyond BACI: sampling designs that might reliably detect environmental disturbances. Ecol Appl 4: 3-15
87. Wild C, Woyt H, Huettel M (2005) Influence of coral mucus on nutrient fluxes in carbonate sands. Mar Ecol Prog Ser 287: 87-98 (Pubitemid 40428432)
88. 2 availabil-ity. Mar Ecol Prog Ser411: 61-71
89. Wild C, Hoegh-Guldberg O, Naumann MS, Colombo-Pallotta MF and others (2011) Climate change impedes scleractinian corals as primary reef ecosystem engineers. Mar Freshw Res 62: 205-215
90. Wooldridge SA (2009) A new conceptual model for the enhanced release of mucus in symbiotic reef corals dur-ing 'bleaching' conditions. Mar Ecol Prog Ser 396: 145-152
91. Yahel R, Yahel G, Genin A (2005) Near-bottom depletion of zooplankton over coral reefs. I. Diurnal dynamics and size distribution. Coral Reefs 24: 75-85