Journal of Applied Phycology

, Volume 29, Issue 3, pp 1683–1693 | Cite as

Interactive effects of nutrient availability, temperature, and irradiance on photosynthetic pigments and color of the brown alga Undaria pinnatifida

  • Hikaru EndoEmail author
  • Yutaka Okumura
  • Yoichi Sato
  • Yukio Agatsuma


Color is one of the important factors that determine the commercial value of cultivated marine macroalgae such as the brown alga Undaria pinnatifida (Laminariales; Phaeophyta) in Japan. Macroalgal color is fundamentally derived from the algal photosynthetic pigment content, which is affected by abiotic factors. However, little is known about the quantitative relationship between pigment content and color and the direct effects of abiotic factors on the color of marine macroalgae. We conducted a 24-day indoor culture experiment to assess the combined effects of nutrient availability (enriched and nonenriched seawater), seawater temperature (15 and 5 °C), and irradiance (180 and 30 μmol photons m−2 s−1) on the concentrations of six pigments (chlorophyll (Chl) a, Chl c 1, Chl c 2, fucoxanthin, violaxanthin, and zeaxanthin) and three color values (lightness L*, redness a*, and yellowness b*) of U. pinnatifida sporophytes. Negative correlations between pigment content and color values of the cultured algae were detected. Reduced nutrient availability, decrease in temperature, and elevated irradiance resulted in decreased pigment contents and increased color values. Moreover, a significant interaction between nutrient availability and temperature indicated that the positive effect of nutrient enrichment was antagonized by a decrease in temperature. These results suggest that U. pinnatifida can discolor under nutrient-poor, winter temperature, and saturated irradiance conditions. To increase the commercial value of this species, artificial nutrient enrichment during spring or cultivation from a deeper depth may be effective.


Nonadditive effect Seaweed aquaculture Commercial value L*a*b* color difference Marine macroalgae 



We thank Dr. M. Aoki of Tohoku University for providing discolored specimens of the kelp U. pinnatifida collected in Miyagi Prefecture. This work was supported by the project “Tohoku Ecosystem-Associated Marine Sciences (TEAMS).”


  1. Agatsuma Y (1998) Aquaculture of the sea urchin (Strongylocentrotus nudus) transplanted from coralline flats in Hokkaido, Japan. J Shellfish Res 17:1541–1547Google Scholar
  2. Anthony KR, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Aacad Sci USA 105:17442–17446CrossRefGoogle Scholar
  3. Baghdadli D, Tremblin G, Ducher M (1994) The effects of light quality on growth, photosynthesis and development in cultivated thalli of Cystoseira barbata C. Ag. f. aurantia (Kütz.) Giaccone (Phaeophyceae, Fucales). Bot Mar 37:43–50CrossRefGoogle Scholar
  4. Celis-Plà P, Díaz-Caneja BM, Quintano E, García-Sánchez M, Pedersen A, Navarro NP, Copertino MS, Mangaiyarkarasi N, Mariath R, Figueroa FL, Korbee N (2014) Short-term ecophysiological and biochemical responses of Cystoseira tamariscifolia and Ellisolandia elongata to environmental changes. Aquat Biol 22:227–243CrossRefGoogle Scholar
  5. Chapman ARO, Markham JW, Lüning K (1978) Effects of nitrate concentration on the growth and physiology of Laminaria saccharina (Phaeophyta) in culture. J Phycol 14:195–198CrossRefGoogle Scholar
  6. Dan A, Ohno M, Matsuoka M (2015) Changes of the research and development on the resources of Undaria and Laminaria in the culture ground of Tokushima coasts. Bull Tokushima Pref Fish Res Inst 10:25–48 (in Japanese with English abstract)Google Scholar
  7. Davison IR (1987) Adaptation of photosynthesis in Laminaria saccharina (Phaeophyta) to changes in growth temperature. J Phycol 23:273-283Google Scholar
  8. Davison IR (1991) Environmental effects on algal photosynthesis: temperature. J Phycol 27:2–8CrossRefGoogle Scholar
  9. Dean PR, Hurd CL (2007) Seasonal growth, erosion rates, and nitrogen and photosynthetic ecophysiology of Undaria pinnatifida (Heterokontophyta) in southern New Zealand. J Phycol 43:1138–1148CrossRefGoogle Scholar
  10. Demmig-Adams B, Gilmore AM, Adams W (1996) Carotenoids 3: in vivo function of carotenoids in higher plants. FASEB J 10:403–412PubMedGoogle Scholar
  11. Drew EA (1983) Physiology of Laminaria. I. Use of excised lamina discs in short and long term experiments. PSZNI Mar Ecol 4:227–250CrossRefGoogle Scholar
  12. Figueroa FL, Israel A, Neori A, Martínez B, Malta EJ, Ang P Jr, Inken S, Marquardt R, Korbee N (2009) Effects of nutrient supply on photosynthesis and pigmentation in Ulva lactuca (Chlorophyta): responses to short-term stress. Aquat Biol 7:173–183CrossRefGoogle Scholar
  13. Figueroa FL, Israel A, Neori A, Martínez B, Malta EJ, Ang P Jr, Inken S, Marquardt R, Abdala R, Korbee N (2010) Effect of nutrient supply on photosynthesis and pigmentation to short-term stress (UV radiation) in Gracilaria conferta (Rhodophyta). Mar Poll Bull 60:1768–1778CrossRefGoogle Scholar
  14. Flukes EB, Wright JT, Johnson CR (2015) Phenotypic plasticity and biogeographic variation in physiology of habitat-forming seaweed: response to temperature and nitrate. J Phycol 51:896–909CrossRefPubMedGoogle Scholar
  15. Gao X, Endo H, Yamana M, Taniguchi K, Agatsuma Y (2013a) Compensation of the brown alga Undaria pinnatifida (Laminariales; Phaeophyta) after thallus excision under cultivation in Matsushima Bay, northern Japan. J Appl Phycol 25:1171–1178CrossRefGoogle Scholar
  16. Gao X, Endo H, Taniguchi K, Agatsuma Y (2013b) Combined effects of seawater temperature and nutrient condition on growth and survival of juvenile sporophytes of the kelp Undaria pinnatifida (Laminariales; Phaeophyta) cultivated in northern Honshu, Japan. J Appl Phycol 25:269–275CrossRefGoogle Scholar
  17. Gao X, Endo H, Yamana M, Taniguchi K, Agatsuma Y (2013c) Compensatory abilities depending on seasonal timing of thallus excision of the kelp Undaria pinnatifida cultivated in Matsushima Bay, northern Japan. J Appl Phycol 25:1331–1340CrossRefGoogle Scholar
  18. Gao X, Endo H, Taniguchi K, Agatsuma Y (2013d) Genetic differentiation of high-temperature tolerance in the kelp Undaria pinnatifida sporophytes from geographically separated populations along the Pacific coast of Japan. J Appl Phycol 25:567–574CrossRefGoogle Scholar
  19. Gerard VA (1997) The role of nitrogen nutrition in high-temperature tolerance of the kelp, Laminaria saccharina (Chromophyta). J Phycol 33:800–810CrossRefGoogle Scholar
  20. Hurd CL, Harrison PJ, Bischof K, Lobban CS (2014) Seaweed ecology and physiology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  21. Kobayashi M, Fujita D (2014) Can thallus color of red algae be used as an environmental indicator in shallow waters? J Appl Phycol 26:1123–1131CrossRefGoogle Scholar
  22. Lapointe BE, Tenore KR, Dawes CJ (1984a) Interactions between light and temperature on the physiological ecology of Gracilaria tikvahiae (Gigartinales: Rhodophyta). II. Nitrate uptake and levels of pigments and chemical constituents. Mar Biol 80:171–178CrossRefGoogle Scholar
  23. Lapointe BE, Tenore KR, Dawes CJ (1984b) Interactions between light and temperature on the physiological ecology of Gracilaria tikvahiae (Gigartinales: Rhodophyta). I. Growth, photosynthesis and respiration. Mar Biol 80:161–170CrossRefGoogle Scholar
  24. Lopez-Figueroa F (1991) Control by light quality of chlorophyll synthesis in the brown alga Desmarestia aculeata. Z Naturforsch 46:542–548Google Scholar
  25. López-Figueroa F, Niell FX (1990) Effects of light quality on chlorophyll and biliprotein accumulation in seaweeds. Mar Biol 104:321–327CrossRefGoogle Scholar
  26. Lotze HK, Worm B (2002) Complex interactions of climatic and ecological controls on macroalgal recruitment. Limnol Oceanogr 47:1734–1741CrossRefGoogle Scholar
  27. MacIntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria. J Phycol 38:17–38CrossRefGoogle Scholar
  28. Makino K, Sumitomo T, Nakanishi T, Kato S, Hirano T, Ueta Y (2015) Mechanism of and counter-measures against discoloration of cultured wakame Undaria pinnatifida. Aquabiology 37:254–260 (in Japanese)Google Scholar
  29. McBride SC, Price RJ, Tom PD, Lawrence JM, Lawrence AL (2004) Comparison of gonad quality factors: color, hardness and resilience, of Strongylocentrotus franciscanus between sea urchins fed prepared feed or algal diets and sea urchins harvested from the Northern California fishery. Aquaculture 233:405–422CrossRefGoogle Scholar
  30. McGlathery KJ, Pedersen MF (1999) The effect of growth irradiance on the coupling of carbon and nitrogen metabolism in Chaetomorpha linum (Chlorophyta). J Phycol 35:721–731CrossRefGoogle Scholar
  31. Murayama F, Shimizu Y, Takagi S (2015) The relationships between nutrient concentration in the coastal area of Okayama prefecture, the color tone of fresh thalli (Pyropia) and the unit price of dried nori. Nippon Suisan Gakk 81:107–114 (in Japanese with English abstract)CrossRefGoogle Scholar
  32. Niwa K, Harada K (2013) Physiological responses to nitrogen deficiency and resupply in different blade portions of Pyropia yezoensis f. narawaensis (Bangiales, Rhodophyta). J Exp Mar Biol Ecol 439:113–118CrossRefGoogle Scholar
  33. Perez-Bermudez P, Garcia-Carrascosa M, Cornejo MJ, Segura J (1981) Water-depth effects in photosynthetic pigment content of the benthic algae Dictyota dichotoma and Udotea petiolata. Aquat Bot 11:373–377CrossRefGoogle Scholar
  34. Peteiro C, Sánchez N, Martínez B (2016) Mariculture of the Asian kelp Undaria pinnatifida and the native kelp Saccharina latissima along the Atlantic coast of Southern Europe: an overview. Algal Res 15:9–23CrossRefGoogle Scholar
  35. Ramus J, Lemons F, Zimmerman C (1977) Adaptation of light-harvesting pigments to downwelling light and the consequent photosynthetic performance of the eulittoral rockweeds Ascophyllum nodosum and Fucus vesiculosus. Mar Biol 42:293–303CrossRefGoogle Scholar
  36. Roach DA, Wulff RD (1987) Maternal effects in plants. Annu Rev Ecol Syst 18:209–235CrossRefGoogle Scholar
  37. Sato Y, Hirano T, Niwa K, Suzuki T, Fukunishi N, Abe T, Kawano S (2016a) Phenotypic differentiation in the morphology and nutrient uptake kinetics among Undaria pinnatifida cultivated at six sites in Japan. J Appl Phycol. doi: 10.1007/s10811-016-0857-9 Google Scholar
  38. Sato Y, Yamaguchi M, Hirano T, Fukunishi N, Abe T, Kawano S (2016b) Effect of water velocity on Undaria pinnatifida and Saccharina japonica growth in a novel tank system designed for macro algae cultivation. J Appl Phycol. doi: 10.1007/s10811-016-1013-2 Google Scholar
  39. Sonoike K (2011) Photoinhibition of photosystem I. Physiol plantarum 142:56–64CrossRefGoogle Scholar
  40. Tatewaki M (1966) Formation of a crustaceous sporophyte with unilocular sporangia in Scytosiphon lomentaria. Phycologia 6:62–66CrossRefGoogle Scholar
  41. Uhrmacher S, Hanelt D, Nultsch W (1995) Zeaxanthin content and the degree of photoinhibition are linearly correlated in the brown alga Dictyota dichotoma. Mar Biol 123:159–165CrossRefGoogle Scholar
  42. Umezawa Y, Miyajima T, Yamamuro M, Kayanne H, Koike I (2002) Fine-scale mapping of land-derived nitrogen in coral reefs by δ15N in macroalgae. Limnol Oceanogr 47:1405–1416CrossRefGoogle Scholar
  43. Uwai S, Nelson W, Neill K, Wang WD, Aguilar-Rosas LE, Boo SM, Kitayama T, Kawai H (2006) Genetic diversity in Undaria pinnatifida (Laminariales, Phaeophyceae) deduced from mitochondria genes-origins and succession of introduced populations. Phycologia 45:687–695CrossRefGoogle Scholar
  44. Voisin M, Engel CR, Viard F (2005) Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects. Proc Natl Acad Sci U S A 102:5432–5437CrossRefPubMedPubMedCentralGoogle Scholar
  45. Watanabe Y, Nishihara GN, Tokunaga S, Terada R (2014) The effect of irradiance and temperature responses and the phenology of a native alga, Undaria pinnatifida (Laminariales), at the southern limit of its natural distribution in Japan. J Appl Phycol 26:2405–2415CrossRefGoogle Scholar
  46. Zapata M, Rodriguez F, Garrido JL (2000) Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-containing mobile phases. Mar Ecol Prog Ser 195:29–45CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Graduate School of Agricultural ScienceTohoku UniversitySendaiJapan
  2. 2.Faculty of FisheriesKagoshima UniversityKagoshimaJapan
  3. 3.Tohoku National Fisheries Research InstituteJapan Fisheries Research and Education AgencyShiogamaJapan
  4. 4.Riken Food Co., Ltd.TagajoJapan
  5. 5.RIKEN, Ion Beam BreedingWakoJapan

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