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Taxonomic identity and the effect of temperature and irradiance on the photosynthesis of an indoor tank-cultured red alga Agardhiella subulata from Japan


We determined through morphological and rbcL phylogenetic analyses that a previously unidentified, but introduced species of macroalga, which has been easily cultivated in indoor tanks in Japan, is Agardhiella subulata (Solieriaceae). Additionally, the photosynthetic biology of this alga was examined by inducing photosynthetic activity under a variety of water temperatures and photosynthetic active radiation (PAR) to clarify the optimal conditions needed for its efficient cultivation. Photosynthetic activity was evaluated by using both dissolved oxygen (DO) and pulse amplitude modulated-chlorophyll fluorometric (PAM) techniques, and focused on elucidating temperature and PAR levels that would potentially maximize productivity. The DO method revealed that the net photosynthetic rates at 24 °C quickly increased as PAR increased, and approached a P max of 27.8 mg O2 g −1ww  min−1 (95 % Bayesian credible interval, BCI 23.8–32.1). The maximum gross photosynthetic rate occurred at 26.7 °C (BCI 24.4–28.3 °C). However, PAM experiments indicated that for the maximum quantum yield, the optimal temperature was 23.7 °C (BCI 22.7–24.6) and the maximum relative electron rates occurred when the water temperature was 31.0 °C (BCI 30.6–31.5). This study suggests that the broad tolerance of maximal photosynthetic activity to temperature (22.7–31.5 °C) is one of the main reasons why this alga can be successfully cultivated year-round.

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  1. 1.

    Humm HJ (1962) Marine algae of Virginia as a source of agar and agaroids. Virginia Inst Mar Sci Spec Sci Rep 37:1–13

    Google Scholar 

  2. 2.

    Moeller HW (1964) A standing crop estimate of some marine plants in Barnegat Bay. N J Acad Sci 9:27–30

    Google Scholar 

  3. 3.

    DeBoer JA, Lapointe BE (1976) Effects of culture density and temperature on the growth rate and yield of Neoagardhiella bailey. In: Ryther JH (ed) Marine polyculture based on natural food chains and recycled wastes. Woods Hole Oceanographic Inst., Tech. Rep. WHOI-76-92, p 281

  4. 4.

    Gabrielson PW, Hommersand MH (1982) The morphology of Agardhiella subulata representing the Agardhielleae, a new tribe in the Solieriaceae (Gigartinales, Rhodophyta). J Phycol 18:46–58

    Article  Google Scholar 

  5. 5.

    Gabrielson PW (1985) Agardhiella versus Neoagardhiella (Solieriaceae, Rhodophyta): another look at the lectotypification of Gigartina tenera. Taxon 34:275–280

    Article  Google Scholar 

  6. 6.

    Coon DA, Neushul M, Charters AC (1972) The settling behaviour of marine algal spores. Proc Int Seaweed Symp 7:237–242

    Google Scholar 

  7. 7.

    Okuda T, Neushul M (1981) Sedimentation studies of red algal spores. J Phycol 17:113–118

    Article  Google Scholar 

  8. 8.

    DeBoer JA, Ryther JH (1978) Potential yields from a waste-recycling algal mariculture system. In: Krauss R (ed) The marine plant biomass of the Pacific Northwest Coast. Oregon State University Press, Oregon, pp 231–249

    Google Scholar 

  9. 9.

    Ryther JH, DeBoer JA, Lapointe BE (1978) Cultivation of seaweeds for hydrocolloids, waste treatment and biomass for energy conversion. Proc Int Seaweed Symp 9:1–16

    Google Scholar 

  10. 10.

    Brinkhuis BH, Hanisak MD (1981) Development of a marine biomass program in New York. Int. Gas Res. Conf., pp 682–692

  11. 11.

    DeBoer JA (1978) Effects of nitrogen enrichment on growth rate and phycocolloid content in Gracilaria foliifera and Neoagardhiella baileyi (Florideophyceae). Proc Int Seaweed Symp 9:263–271

    Google Scholar 

  12. 12.

    Kursar TA, Alberte RS (1983) Photosynthetic unit organization in a red alga. Relationships between light-harvesting pigments and reaction centers. Plant Physiol 72:409–414

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  13. 13.

    Huang YM, Maliakal S, Cheney DP, Rorrer GL (1998) Comparison of development and photosynthetic growth for filament clumps and regenerated microplantlet cultures of Agardhiella subulata (Rhodophyta, Gigartinales). J Phycol 34:893–901

    Article  Google Scholar 

  14. 14.

    Cheney DP, Luistro AH, Bradley PM (1987) Carrageenan analysis of tissue cultures and whole plants of Agardhiella subulata. Hydrobiologia 151/152:161–166

    Article  Google Scholar 

  15. 15.

    Taylor WR (1960) Marine algae of the eastern tropical and subtropical coasts of the Americas. The University of Michigan Press, Michigan

    Google Scholar 

  16. 16.

    Price, JH, John, DM, Lawson, GW (1986). Seaweeds of the western coast of tropical Africa and adjacent islands: a critical assessment. IV. Rhodophyta (Florideae). 1. Genera A-F. Bull Br Museum (Natural History) Bot 15:1–122

    Google Scholar 

  17. 17.

    Schneider CW, Searles RB (1991) Seaweeds of the southeastern United States. Cape Hatteras to Cape Canaveral. Duke University Press, Durham

    Google Scholar 

  18. 18.

    Verlaque M (2001) Checklist of the macroalgae of Thau Lagoon (Hérault, France), a hot spot of marine species introduction in Europe. Oceanol Acta 24:29–49

    Article  Google Scholar 

  19. 19.

    Perrone C, Cecere E (1994) Two solieriacean algae new to the Mediterranean—Agardhiella subulata and Solieria filiformis (Rhodophyta, Gigartinales). J Phycol 30:98–108

    Article  Google Scholar 

  20. 20.

    Manghisi A, Logorelli F, Morabito M (2008) Agardhiella subulata (C. Agardh) Kraft et M.J. Wynne (Solieriaceae, Rhodophyta), a new introduction in lake Ganzirri (Messina, Sicily). In: 103° Congresso della Società Botanica Italiana. Reggio Calabria, p 75

  21. 21.

    Manghisi A, Morabito M, Bertuccio C, Le Gall L, Couloux A, Cruaud C, Genovese G (2010) Is routine DNA barcoding an efficient tool to reveal introductions of alien macroalgae? A case study of Agardhiella subulata (Solieriaceae, Rhodophyta) in Cape Peloro lagoon (Sicily, Italy). Crypt Algol 34:423–433

    Google Scholar 

  22. 22.

    Sudo Y, Uchizato R, Toma T (2002) Study of the land based aquaculture of Gracilaria I. Annu Bull Okinawa Deep Sea Water Res Cent 1:65–70 (in Japanese)

    Google Scholar 

  23. 23.

    Toma T (2012) Seaweed and seagrass of Okinawa (Natural habitat, cultivation and 250 species of seaweeds). Mugen, Naha (in Japanese)

    Google Scholar 

  24. 24.

    Shimada S, Hiraoka M, Nabata S, Iima M, Masuda M (2003) Molecular phylogenetic analyses of the Japanese Ulva and Enteromorpha (Ulvales, Ulvophyceae), with special reference to the free-floating Ulva. Phycol Res 51:99–108

    Article  CAS  Google Scholar 

  25. 25.

    Shimada S, Yokoyama N, Arai S, Hiraoka M (2009) Phylogeography of the genus Ulva (Ulvophyceae, Chlorophyta), with special reference to the Japanese freshwater and brackish taxa. J Appl Phycol 20:529–539

    Google Scholar 

  26. 26.

    Faye EJ, Kogame K, Shimada S, Kawaguchi S, Masuda M (2008) New red alga Meristotheca imbricata (Solieriaceae, Gigartinales) from Japan. Phycol Res 56:115–126

    Article  Google Scholar 

  27. 27.

    Tanabe AS (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol Ecol Res 11:914–921

    Article  Google Scholar 

  28. 28.

    Jobb G, von Haeseler A, Strimmer K (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4:18

    PubMed Central  PubMed  Article  Google Scholar 

  29. 29.

    Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  30. 30.

    Terada R, Inoue S, Nishihara GN (2013) The effect of light and temperature on the growth and photosynthesis of Gracilariopsis chorda (Gracilariales, Rhodophyta) from geographically separated locations of Japan. J Appl Phycol 25:1863–1872

    Article  CAS  Google Scholar 

  31. 31.

    Nishihara GN, Terada R, Noro T (2004) Photosynthesis and growth rates of Laurencia brongniartii J. Agardh (Rhodophyta, Ceramiales) in preparation for cultivation. J Appl Phycol 16:303–308

    Article  Google Scholar 

  32. 32.

    Muraoka D, Yamamoto H, Yasui H, Terada R (1998) Formation of wound tissue of Gracilaria chorda Holmes (Gracilaceae) in culture. Bull Fac Fish Hokkaido Univ 49:31–39

    Google Scholar 

  33. 33.

    Serisawa Y, Yokohama Y, Aruga Y, Tanaka J (2001) Photosynthesis and respiration in bladelet of Ecklonia cava Kjellman (Laminariales, Phaeophyta) in two localities with different temperature conditions. Phycol Res 49:1–11

    Article  CAS  Google Scholar 

  34. 34.

    Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547

    Article  CAS  Google Scholar 

  35. 35.

    Henley WJ (1993) Measurement and interpretation of photosynthetic light-response curves in algae in the context of photo inhibition and diel changes. J Phycol 29:729–739

    Article  Google Scholar 

  36. 36.

    Lideman, Nishihara GN, Noro T, Terada R (2013) Effect of temperature and light on the photosynthesis as measured by chlorophyll fluorescence of cultured Eucheuma denticulatum and Kappaphycus sp. (Sumba strain) from Indonesia. J Appl Phycol 25:399–406

  37. 37.

    Gelman A, Jakulin A, Pittau MG, Su YS (2008) A weakly informative default prior distribution for logistic and other regression models. Ann Appl Stat 2:1360–1383

    Article  Google Scholar 

  38. 38.

    Tsuchiya Y, Nishihara GN, Terada R (2012) Photosynthetic and temperature characteristics of five Sargassum species (Fucales), S. piluliferum, S. patens, S. fusiforme, S. crispifolium, S. alternato-pinnatum from Kagoshima, Japan, using dissolved oxygen sensor and pulse-amplitude-modulated (PAM) fluorometer. Nippon Suisan Gakkaishi 78:189–197 (in Japanese)

    Article  Google Scholar 

  39. 39.

    Alexandrov GA, Yamagata Y (2007) A peaked function for modeling temperature dependence of plant productivity. Ecol Model 200:189–192

    Article  Google Scholar 

  40. 40.

    Ralph PJ, Burchett MD (1995) Photosynthetic responses of the seagrass Halophila ovalis (R. Br.) Hook. f. to high irradiance stress, using chlorophyll a fluorescence. Aquat Bot 51:55–66

    Article  CAS  Google Scholar 

  41. 41.

    Ralph PJ, Gademann R, Dennison WC (1998) In situ seagrass photosynthesis measured using a submersible, pulse-amplitude modulated fluorometer. Mar Biol 132:367–373

    Article  Google Scholar 

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We express our gratitude to Masayuki Yamada, Okinawa Prefectural Fisheries Research and Extension Center, and Miyuki Manabe, Kagoshima Prefectural Fisheries Technology and Development Center, for their kind suggestions and preparation of the materials. We also thank Takahiro Kurahori, Soku Shikada, and Yoshiaki Kitamura, Kagoshima University, for their kind assistance to complete the experiments. This study was supported in part by a Scientific Grant-in-Aid for Scientific Research (#22510033 and #25340012) from the Japanese Ministry of Education, Science, Sports and Culture (RT and GNN) and by the JSPS RONPAKU (Dissertation PhD) Program (TDV) from the Japan Society for the Promotion of Science (JSPS).

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Correspondence to Ryuta Terada.

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Vo, T.D., Nishihara, G.N., Shimada, S. et al. Taxonomic identity and the effect of temperature and irradiance on the photosynthesis of an indoor tank-cultured red alga Agardhiella subulata from Japan. Fish Sci 80, 281–291 (2014).

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  • Agardhiella subulata
  • Algae
  • Photosynthesis
  • PAM fluorometry