Seasonal photoacclimation patterns in the intertidal macroalga cystoseira tamariscifolia (ochrophyta);Patrones estacionales de fotoaclimatación en el alga intermareal, Cystoseira tamariscifolia (Ochrophyta)

Scientia Marina

Volumn 78, Issue 3, 2014, Pages 377-388

  Celis Plá, Paula S M ^a,b   Korbee, Nathalie ^a   Gómez Garreta, Amelia ^b   Figueroa, Félix L ^a  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Antioxidant activity; Cystoseira tamariscifolia; Phenolic compounds; Photoinhibition; Photoprotection

Indexed keywords

ACCLIMATION; ANTIOXIDANT; INTERTIDAL COMMUNITY; MACROALGA; PHENOLIC COMPOUND; PHOTOINHIBITION; PHOTOPROTECTION; PHOTOSYNTHESIS;

SPAIN;

ALGAE; CYSTOSEIRA TAMARISCIFOLIA; STRAMENOCHROMA;

EID: 84907797754     PISSN: 02148358     EISSN: 18868134     Source Type: Journal    
DOI: 10.3989/scimar.04053.05A     Document Type: Article

References (69)

1. Abdala-Díaz R.T., Cabello-Pasini A., Pérez-Rodríguez E., et al. 2006. Daily and seasonal variations of optimum quantum yield and phenolic compounds in Cystoseira tamariscifolia (Phaeophyta). Mar. Biol. 148: 459-465. http://dx.doi.org/10.1007/s00227-005-0102-6
2. Amsler C.D., Fairhead V.A. 2006. Defensive and sensory chemical ecology of brown algae. Adv. Bot. Res. 43: 1-91. http://dx.doi.org/10.1016/S0065-2296(05)43001-3
3. Arévalo R., Pinedo S., Ballesteros E. 2007. Changes in the composition and structure of Mediterranean rocky-shore communities following a gradient of nutrient enrichment: descriptive study and test of proposed methods to assess water quality regarding macroalgae. Mar. Pollut. Bull. 55: 104-113. http://dx.doi.org/10.1016/j.marpolbul.2006.08.023
4. Ballesteros E., Torras X., Pinedo S., et al. 2007. A new methodology based on littoral community cartography dominated by macroalgae for the implementation of the European Water Framework Directive. Mar. Pollut. Bull. 55: 172-180. http://dx.doi.org/10.1016/j.marpolbul.2006.08.038
5. Belshe E.F., Durako M.J., Blum J.E. 2007. Photosynthetic rapid light curves (RLC) of Thalassia testudinum exhibit diurnal variation. J. Exp. Mar. Biol. Ecol. 342: 253-268. http://dx.doi.org/10.1016/j.jembe.2006.10.056
6. Bischof K., Gómez I., Molis M., et al. 2006. Ultraviolet radiation shapes seaweed communities. Rev. Environ. Sci. Biotechnol. 5: 141-166. http://dx.doi.org/10.1007/s11157-006-0002-3
7. Blois M.S. 1958. Antioxidant determinations by the use of a stable free radical. Nature 181: 1199-1200. http://dx.doi.org/10.1038/1811199a0
8. Cabello-Pasini A., Macías-Carranza V., Abdala R., et al. 2011. Effect of nitrate concentration on UVR on photosynthesis, respiration, nitrate reductase activity and phenolic compounds in Ulva rigida (Chlorophyta). J. Appl. Phycol. 23: 363-369. http://dx.doi.org/10.1007/s10811-010-9548-0
9. Carlson D.J., Carlson M.L. 1984. Reassessment of exudation by fucoid macroalgae. Limnol. Oceanogr. 29: 1077-1084. http://dx.doi.org/10.4319/lo.1984.29.5.1077
10. Celis-Plá P., Martínez B., Quintano E., et al. 2014. Short-term ecophysiological and biochemical responses of Cystoseira tamariscifolia and Ellisolandia elongata to enviromental changes. Aquat. Biol. In press. http://dx.doi.org/10.3354/ab00573
11. Connan S., Goulard F., Stiger V., et al. 2004. Interspecific and temporal variation in phlorotannin levels in an assemblage of brown algae. Bot. Mar. 47: 410-416. http://dx.doi.org/10.1515/BOT.2004.057
12. Connan S., Delisle F., Deslandes E., et al. 2006. Intra-thallus phlorotannin content and antioxidant activity in Phaeophyceae of temperate waters. Bot. Mar. 49: 39-46. http://dx.doi.org/10.1515/BOT.2006.005
13. Craigie J.S., McLachlan J. 1964. Excretion of coloured ultraviolet absorbing substances by marine algae. Can. J. Bot. 42: 23-33. http://dx.doi.org/10.1139/b64-003
14. Cruces E., Huovinen P., Gómez I. 2012. Phlorotannin and antioxidant responses upon short-term exposure to UV radiation and elevated temperature in three south Pacific kelps. Photochem. Photobiol. 88: 58-66. http://dx.doi.org/10.1111/j.1751-1097.2011.01013.x
15. Demmig-Adams B., Adams W.III. 2006. Photoprotection in an ecological context: the remarkable complexity of thermal dissipation. New. Phytologist 172: 11-21. http://dx.doi.org/10.1111/j.1469-8137.2006.01835.x
16. Dring M.J., Brown F.A. 1982. Photosynthesis of intertidal brown algae during and after periods of emersion; a renewed search for physiological case of zonations. Mar. Ecol. Prog. Ser. 8: 301-308. http://dx.doi.org/10.3354/meps008301
17. Dujmov J., Sucevic P., Antolic B. 1996. Spectrofluorometric applications in studying macroalgal exudates. Mar. Ecol. 17: 501-508. http://dx.doi.org/10.1111/j.1439-0485.1996.tb00523.x
18. Falkowski P. G. 1997. Evolution of the nitrogen cycle and its influence on the biological sequestration of C02 in the ocean. Nature 382: 272-275. http://dx.doi.org/10.1038/387272a0
19. Figueroa F.L., Gómez I. 2001. Photoacclimation to solar UV radiation in red macroalgae. J. Appl. Phycology. 13: 235-248. http://dx.doi.org/10.1023/A:1011126007656
20. Figueroa F.L., Korbee N. 2010. Interactive effects of UV radiation and nutrients on ecophysiology: vulnerability and adaptation to climate change. In: Israel A., Einvav R., Seckbach J. (eds), Seaweeds and their role in globally changing environments. Springer, pp. 157-182. http://dx.doi.org/10.1007/978-90-481-8569-6_10
21. Figueroa F.L., Viñegla B. 2001. Effects of solar UV radiation on photosynthesis and enzyme activities (carbonic anhydrase and nitrate reductase) in marine macroalgae from Southern Spain. Rev. Chil. Hist. Nat. 74: 237-249. http://dx.doi.org/10.4067/S0716-078X2001000200003
22. Figueroa F.L., Salles S., Aguilera J., et al. 1997. Effects of solar radiation on photoinhibition and pigmentation in the red alga Porphyra leucosticta. Mar. Ecol. Prog. Ser. 151: 81-90. http://dx.doi.org/10.3354/meps151081
23. Figueroa F.L., Conde-Álvarez R., Gómez I. 2003. Relations between electron transport rates determined by pulse amplitude modulated chlorophyll fluorescence and oxygen evolution in macroalgae under different light conditions. Photosynth. Res. 75: 259-275. http://dx.doi.org/10.1023/A:1023936313544
24. Figueroa F.L., Martínez B., Israel A., et al. 2009. Acclimation of Red Sea macroalgae to solar radiation: photosynthesis and thallus absorptance. Aquat. Biol. 7: 159-172. http://dx.doi.org/10.3354/ab00186
25. Figueroa F.L., Domínguez-González, B., Korbee N. 2014. Vulnerability and acclimation to increased UVB radiation in three intertidal macroalgae of different morpho-funtional groups. Mar. Environ. Res. 97: 30-38. http://dx.doi.org/10.1016/j.marenvres.2014.01.009
26. Flores-Moya A., Gómez I., Viñegla B., et al. 1998. Effects of solar radiation on the endemic Mediterranean red alga Rissoella verrucosa: photosynthetic performance, pigment content and the activities of enzymes related to nutrient uptake. New. Phytol. 139: 673-683. http://dx.doi.org/10.1046/j.1469-8137.1998.00233.x
27. Flores-Moya A., Hanelt D., Figueroa F.L., et al. 1999. Involvement of solar UV-B radiation in recovery of inhibited photosynthesis in the brown alga Dictyota dichotoma (Hudson) Lamouroux. J. Photochem. Photobiol. 49: 29-135.
28. Folin O., Ciocalteu V. 1927. On tyrosine and tryptophane determinations in proteins. J Biol. Chem. 12: 239-243.
29. Gómez I., Huovinen P. 2010. Induction of phlorotannins during UV exposure mitigates inhibition of photosynthesis and DNA damage in the kelp Lessonia nigrencens. Photochem. Photobiol. 86: 1056-1063. http://dx.doi.org/10.1111/j.1751-1097.2010.00786.x
30. Häder D.P., Figueroa F.L. 1997. Photoecophysiology of marine macroalgae. Photochem. Photobiol. 66: 1-14. http://dx.doi.org/10.1111/j.1751-1097.1997.tb03132.x
31. Häder D.P., Lebert M., Figueroa F.L., et al. 1998. Photoinhibition in Mediterranean macroalgae by solar radiation measured on site by PAM fluorescence. Aquat. Bot. 61: 225-236. http://dx.doi.org/10.1016/S0304-3770(98)00068-0
32. Hanelt D. 1996. Photoinhibition of photosynthesis in marine macroalgae. Sci. Mar. 60: 243-248.
33. Hanelt D., Figueroa F.L. 2012. Physiological and photomorphogenic effects of light of marine macrophytes. In: Wienke C., Bischof K. (eds), Seaweed biology. Ecological studies, Springer-Verlag Berlin Heidelberg, pp. 3-23. http://dx.doi.org/10.1007/978-3-642-28451-9_1
34. Hanelt D., Wiencke C., Bischof K. 2003. Photosynthesis in Marine Macroalgae, Photosynthesis in Algae. In: Larkum W.A., Douglas E., Raven J.A. (eds), Advances in Photosynthesis and Respiration. Kluwer Academic Publisher, pp. 413-435.
35. Honkanen T., Jormalainen V. 2002. Within-plant integration and compensation: effects of simulated herbivory on growth and reproduction of the brown alga, Fucus vesiculosus. Int. J. Plant. Sci. 163: 815-823. http://dx.doi.org/10.1086/342081
36. Høiskar B.A.K., Haugen R., Danielsen T., et al. 2003. Multichannel moderate-bandwidth filter instrument for measurement the ozone-column amount, cloud transmittance, and ultraviolet dose rates. Appl. Optics 42: 18-20. http://dx.doi.org/10.1364/AO.42.003472
37. Huovinen P., Leal P., Gómez I. 2010. Interacting effects of copper, nitrogen and ultraviolet radiation on the physiology of three south Pacific kelps. Mar. Freshwater. Res. 61: 330-341. http://dx.doi.org/10.1071/MF09054
38. Jassby A.D., Platt T. 1976. Mathematical Formulation of the Relationship between Photosynthesis and Light for Phytoplankton. Limno. Oceanogr. 21: 540-547. http://dx.doi.org/10.4319/lo.1976.21.4.0540
39. Jennings J. G., Steinberg P. D. 1994. In situ exudation of phlorotannins by the sublittoral kelp Ecklonia radiata. Mar. Biol. 121: 349-354. http://dx.doi.org/10.1007/BF00346744
40. Karban R., Baldwin I.T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago, USA, 329 pp. http://dx.doi.org/10.7208/chicago/9780226424972.001.0001
41. Klughammer C., Schreiber U. 2008. Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. PAM Applications notes. 1: 27-35.
42. Koivikko R., Loponen J., Honkanen T., et al. 2005. Contents of soluble, cell-wall-bound and exuded phlorotannins in the brown alga Fucus vesiculosus, with implications on their ecological functions. J. Chem. Ecol. 31: 195-212. http://dx.doi.org/10.1007/s10886-005-0984-2
43. Korbee N., Figueroa F.L., Aguilera J. 2006. Effect of light quality on the accumulation of photosynthetic pigments, proteins and mycosporine-like amino acids in the red alga Porphyra leucosticta (Bangiales, Rhodophyta). J. Photoch. Photobiol. B. 80: 71-78. http://dx.doi.org/10.1016/j.jphotobiol.2005.03.002
44. Lobban C.S., Harrison P.J. 1994. Seaweed Ecology and Physiology. Cambridge University Press, New York, 367 pp. http://dx.doi.org/10.1017/CBO9780511626210
45. Longstaff B.J., Kildea T., Runcie J.W., et al. 2002. An in situ study of photosynthetic oxygen exchange and electron transport rate in the marine macroalga Ulva lactuca (Chlorophyta). Photosynth. Res. 74: 281-293. http://dx.doi.org/10.1023/A:1021279627409
46. Lüning K. 1990. Seaweeds: Their Environment, Biogeography and Ecophysiology. Wiley, New York, 527 pp.
47. Lüning K., Dring M.J. 1985. Action spectra and spectral quantum yield of photosynthesis in marine macroalgae with thin and thick thalli. Mar. Biol. 87: 119-129. http://dx.doi.org/10.1007/BF00539419
48. Mercado J. M., Gordillo F.J., Figueroa F.L., et al. 1998. External carbonic anhydrase and affinity to inorganic carbon in intertidal macroalgae. J. Exp. Mar. Biol. Ecol. 221: 209-220. http://dx.doi.org/10.1016/S0022-0981(97)00127-5
49. Nitschke U., Connan S., Stengel D. 2012. Chlorophyll a fluorescence responses of temperate Phaeophyceae under submersion and emersion regimes: a comparison of a rapid and steady-state light curves. Photosynth. Res. 114: 29-42. http://dx.doi.org/10.1007/s11120-012-9776-z
50. Nygard C.A., Dring M.J. 2008. Influence of salinity, temperature and dissolved inorganic carbon and nutrient concentration on the photosynthesis and growth of Fucus vesiculosus form Baltic and Irish Sea. Eur. J. Phycol. 43: 253-262. http://dx.doi.org/10.1080/09670260802172627
51. Osmond C.B. 1994. What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker N.R., Bowyer J.R. (eds) Photoinhibition of photosynthesis, from molecular mechanisms to the field. Bios Scientific Publ Oxford, Oxford, pp. 1-24.
52. Pavia H., Toth G.B. 2000. Influence of nitrogen on the phlorotannin content of the brown seaweeds Ascophyllum nodosum and Fucus vesiculosus. Hydrobiologia 440: 299-305. http://dx.doi.org/10.1023/A:1004152001370
53. Pavia H., Cervin G., Lindgren A., et al. 1997. Effects of UVB radiation and simulated herbivory on phlorotannins in the brown alga Ascophylum nodosum. Mar. Ecol. Prog. Ser. 157: 139-146. http://dx.doi.org/10.3354/meps157139
54. Platt T., Gallegos C.L. 1980. Modelling primary production. In: Falkowski P. (eds) Primary Productivity in the Sea. Plenum Press, New York, pp. 339-362. http://dx.doi.org/10.1007/978-1-4684-3890-1_19
55. Peckol P., Krane J. M., Yates J.L. 1996. Interactive effects of inducible defense and resource availability on phlorotannins in the North Atlantic brown alga Fucus vesiculosus. Mar. Ecol. Prog. Ser. 138: 209-217. http://dx.doi.org/10.3354/meps138209
56. Ragan M.A., Craige A. 1980. Quantitative studies on brown algal phenols IV. Ultraviolet spectrophotometry of extracted polyphenols and implications for measuring dissolved organic matter in sea water. J. Exp. Mar. Biol. Ecol. 46: 231-239. http://dx.doi.org/10.1016/0022-0981(80)90033-7
57. Ragan M.A., Jensen A. 1978. Quantitative studies on brown algal phenols II. Seasonal variation in polyphenol content of Ascophyllum nodosum (L.) Le Jol. and Fucus vesiculosus (L) J. Exp. Mar. Biol. Ecol. 34: 245-258. http://dx.doi.org/10.1016/S0022-0981(78)80006-9
58. Ramírez T., Cortés D., Mercado J.M., et al. 2005. Seasonal dynamics of inorganic nutrients and phytoplankton biomass in the NW Alboran Sea. Estuar. Coast. Shelf. Sci. 65: 654-670. http://dx.doi.org/10.1016/j.ecss.2005.07.012
59. Ritchie R.J. 2008. Universal chlorophyll equations for estimating chlorophylls a, b, c and d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol, or ethanol solvents. Photosynthetica 46: 115-126. http://dx.doi.org/10.1007/s11099-008-0019-7
60. Roleda M.Y., Clayton M.N., Wiencke C. 2006. Screening capacity of UV-absorbing compounds in spores of Arctic Laminariales. J. Exp. Mar. Biol. Ecol. 338: 123-133. http://dx.doi.org/10.1016/j.jembe.2006.07.004
61. Sales M., Ballesteros E. 2012. Seasonal dynamics and annual production of Cystoseira crinita (Fucales: Ochrophyta) dominated assemblages from the northwestern Mediterranean. Sci. Mar. 76: 391-401. http://dx.doi.org/10.3989/scimar.03465.16D
62. Schreiber U., Schliwa U., Bilger W. 1986.Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth. Res. 10: 51-62. http://dx.doi.org/10.1007/BF00024185
63. Schreiber U., Endo T., Mi H., et al. 1995. Quenching analysis of chlorophyll fluorescence by saturation pulse method: particular aspects relating to the study of eukaryotic algae and cyanobacteria. Plant. Cell. Physiol. 36: 873-882.
64. Swanson A., Druehl L.D. 2002. Induction, exudation and the UV protective role of kelp phlorotannins. Aquat. Bot. 73: 241-253. http://dx.doi.org/10.1016/S0304-3770(02)00035-9
65. Targett N.M., Coen L.D., Boettcher A.A., et al. 1992. Biogeographic comparisons of marine algal polyphenolics: evidence against a latitudinal trend. Oecologia 89: 464-470.
66. Thibaut T., Pinedo S., Torras X., et al. 2005. Long-term decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Albères coast (France), north-western Mediterranean). Mar. Pollut. Bull. 50: 1472-1489. http://dx.doi.org/10.1016/j.marpolbul.2005.06.014
67. Toth G. B., Pavia H. 2000. Water-borne cues induce chemical defense in a marine alga (Ascophyllum nodosum). Proc. Natl. Acad. Sci. USA 97: 14418-14420. http://dx.doi.org/10.1073/pnas.250226997
68. Underwood A.J. 1997. Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge, New York, 509 pp.
69. Zubia M., Payri C., Deslandes E. 2008. Alginate, mannitol, phenolic compounds and biological activities of two range-extending brown algae, Sargassum mangarevense and Turbinaria ornata (Phaeophyta: Fucales), from Tahiti (French Polynesia). J. Appl. Phycol. 20: 1033-1043. http://dx.doi.org/10.1007/s10811-007-9303-3