Advertisement

Fisheries Science

, Volume 80, Issue 4, pp 695–703 | Cite as

The effect of irradiance and temperature on the photosynthesis of two agarophytes Gelidium elegans and Pterocladiella tenuis (Gelidiales) from Kagoshima, Japan

  • Midori Fujimoto
  • Gregory N. Nishihara
  • Ryuta TeradaEmail author
Original Article Biology

Abstract

The effect of irradiance and temperature on the photosynthesis of two Japanese agarophytes, Gelidium elegans and Pterocladiella tenuis (Gelidiales), was determined using dissolved oxygen sensors and pulse amplitude modulated (PAM) fluorometry. Gross photosynthesis and dark respiration rates were determined over a range of temperatures (8–36 °C). The highest gross photosynthetic rates were 40.3 and 37.0 mg O2 g ww −1  min−1 and occurred at 24.3 and 25.5 °C [95 % Bayesian credible interval (BCI) 20.7–28.0 and 23.4–28.3 °C], respectively. The dark respiration rate in G. elegans and P. tenuis increased with increasing temperature at a rate of 0.10 and 0.31 mg O2 g ww −1  min−1 °C−1 , respectively. Modeling the net photosynthesis–irradiance (PE) responses of G. elegans and P. tenuis at 20 °C revealed that the net photosynthetic rates quickly increased at irradiance levels below the estimated saturation irradiance of 88 and 83 µmol photons m−2 s−1, with a compensation irradiance of 14 and 19 µmol photons m−2 s−1, respectively. The highest value of the maximum effective quantum yield (Φ PSII) occurred at 20.1 °C (BCI 18.9–21.5 °C) and 21.3 °C (BCI 20.2–22.5 °C) for G. elegans and P. tenuis and was 0.49 and 0.45, respectively. These optimal temperatures of Φ PSII were relatively lower than those determined by the photosynthesis–temperature model of oxygen evolution. The temperature response of these species indicates that they are probably well adapted to the current range of seawater temperatures in the study site but that they are near the boundary of their tolerable limits.

Keywords

Agar Algae Gelidium elegans Photosynthesis Pterocladiella tenuis Pulse amplitude modulated (PAM) chlorophyll fluorometry Temperature tolerance 

Notes

Acknowledgments

This research was sponsored in part by a Grant-in-Aid for Scientific Research (#22510033, #25340012 and #25450260) from the Japanese Ministry of Education, Culture, Sport and Technology (RT and GNN).

References

  1. 1.
    Ohno M, Largo DB (1998) The seaweed resources of Japan. In: Critchley AT, Ohno M (eds) Seaweed resources of the World. Japan International Cooperation Agency (JICA), Yokosuka, pp 1–14Google Scholar
  2. 2.
    Zemke-White WL, Ohno M (1999) World seaweed utilisation: an end-of-century summary. J Appl Phycol 11:369–376CrossRefGoogle Scholar
  3. 3.
    Fujita D (2004) Gelidiales. In: Ohno M (ed) Biology and technology of economic seaweeds. Uchida Rohkakuho, Tokyo, pp 201–225 (in Japanese)Google Scholar
  4. 4.
    Akatsuka I (1986) Japanese Gelidiales (Rhodophyta) especially Gelidium. In: Barnes H, Barnes M (eds) Oceanography and marine biology—an annual review, vol 24. Aberdeen University Press, Aberdeen, pp 171–263Google Scholar
  5. 5.
    Yoshida T (1998) Marine algae of Japan. Uchida Rokakuho Publishing, Tokyo (in Japanese)Google Scholar
  6. 6.
    Shimada S, Horiguchi T, Masuda M (2000) Confirmation of the status of three Pterocladia species (Gelidiales, Rhodophyta) described by K. Okamura. Phycologia 39:10–18CrossRefGoogle Scholar
  7. 7.
    Shimada S, Masuda M (2002) Japanese species of Pterocladiella Santelices et Hommersand (Rhodophyta, Gelidiales). In: Abbott IA, Mcdermid KJ (eds) Taxonomy of economic seaweeds with reference to some Pacific species, vol 8. California Sea Grant College, La Jolla, pp 167–181Google Scholar
  8. 8.
    Shimada S, Masuda M (2003) Reassessment of the taxonomic status of Gelidium subfastigiatum (Gelidiales, Rhodophyta). Phycol Res 51:271–278CrossRefGoogle Scholar
  9. 9.
    Yoshida T, Yoshinaga K (2010) Checklist of marine algae of Japan (revised in 2010). Jpn J Phycol 58:69–122 (in Japanese)Google Scholar
  10. 10.
    Japanese Ministry of Environment (1994) Fourth national survey on the natural environment. Biodiversity center of Japan, Ministry of Environment, Fujiyoshida. Available at: http://www.biodic.go.jp/english/J-IBIS.html (in Japanese)
  11. 11.
    Japan Metrological Agency (2013) Long-term trends in sea surface temperature (Northern East China Sea, Japan). Available at: http://www.data.kishou.go.jp/kaiyou/db/nagasaki/nagasaki_warm/nagasaki_warm_areaC.html#title (in Japanese)
  12. 12.
    Japan Metrological Agency (2011) Sea surface temperature in Japan. Available at: http://www.data.kishou.go.jp/kaiyou/db/kaikyo/knowledge/sst.html (in Japanese)
  13. 13.
    Shimabukuro H, Higuchi F, Terada R, Noro T (2007) Seasonal changes of two Sargassum species: S. yamamotoi and S. kushimotense (Fucales, Phaeophyceae) at Shibushi Bay, Kagoshima, Japan. Nippon Suisan Gakkaishi 73:244–249 (in Japanese)CrossRefGoogle Scholar
  14. 14.
    Shimabukuro H, Terada R, Sotobayashi J, Nishihara GN, Noro T (2007) Phenology of Sargassum duplicatum (Fucales, Phaeophyceae) from the southern coast of Satsuma Peninsula, Kagoshima, Japan. Nippon Suisan Gakkaishi 73:454–460 (in Japanese)CrossRefGoogle Scholar
  15. 15.
    Tsuchiya Y, Sakaguchi Y, Terada R (2011) Phenology and environmental characteristics of four Sargassum species (Fucales): S. piluliferum, S. patens, S. crispifolium, and S. alternato-pinnatum from Sakurajima, Kagoshima Bay, southern Japan. Jpn J Phycol 59:1–8 (in Japanese)Google Scholar
  16. 16.
    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. doi: 10.1007/s10811-014-0264-z PubMedCentralPubMedGoogle Scholar
  17. 17.
    Watanabe Y, Nishihara GN, Tokunaga S, Terada R (2014) The effect of irradiance and temperature on the photosynthesis of a cultivated red alga, Pyropia tenera (=Porphyra tenera), at the southern limit of distribution in Japan. Phycol Res. doi: 10.1111/pre.12053 Google Scholar
  18. 18.
    Tanaka T, Yoshimitsu S, Imayoshi Y, Ishiga Y, Terada R (2013) Distribution and characteristics of seaweed/seagrass community in Kagoshima Bay, Kagoshima Prefecture, Japan. Nippon Suisan Gakkaishi 79:20–30 (in Japanese)CrossRefGoogle Scholar
  19. 19.
    Ogata E, Matsui T (1965) Photosynthesis in several marine plants of Japan as affected by salinity, drying and pH, with attention to their growth habitats. Bot Mar 8:199–217CrossRefGoogle Scholar
  20. 20.
    Yokohama Y (1973) A comparative study on photosynthesis temperature relationships and their seasonal changes in marine benthic algae. Int Rev Ges Hydrobiol Hydrogr 58:463–472CrossRefGoogle Scholar
  21. 21.
    Maegawa M, Sugiyama A (1995) Relationship between heat tolerance and the vertical distribution of intertidal algae. Suisanzoshoku 43:429–435 (in Japanese)Google Scholar
  22. 22.
    Katada M (1955) Studies on the propagation of Gelidium. J Shimonoseki College Fish 5:1–87 (in Japanese)Google Scholar
  23. 23.
    Yamazaki H (1962) Studies on the propagation of Gelidiaceous algae. Bull Izu Branch Shizuoka Prefect Fish Exp Stn 19:1–92 (in Japanese)Google Scholar
  24. 24.
    Baba M (2010) Effects of temperature, irradiance and salinity on the growth of Gelidium elegans (Rhodophyta) in laboratory culture. Rep Mar Ecol Res Inst 13:61–74 (in Japanese)Google Scholar
  25. 25.
    Gómez I, Figueroa FL (1998) Effects of solar UV stress on chlorophyll fluorescence kinetics of intertidal macroalgae from southern Spain: a case study in Gelidium species. J Appl Phycol 10:285–294CrossRefGoogle Scholar
  26. 26.
    Mercado JM, Carmona R, Niell X (1998) Bryozoans increase available CO2 for photosynthesis in Gelidium sesquipedale (Rhodophyceae). J Phycol 34:925–927CrossRefGoogle Scholar
  27. 27.
    Silva J, Santos R, Serôdio J, Melo RA (1998) Light response curves for Gelidium sesquipedale from different depths, determined by two methods: O2 evolution and chlorophyll fluorescence. J Appl Phycol 10:295–301CrossRefGoogle Scholar
  28. 28.
    Schmidt EC, dos Santos RW, de Faveri C, Horta PA, de Paula Martins R, Latini A, Ramlov F, Maraschin M, Bouzon ZL (2012) Response of the agarophyte Gelidium floridanum after in vitro exposure to ultraviolet radiation B: changes in ultrastructure, pigments, and antioxidant systems. J Appl Phycol 24:1341–1352CrossRefGoogle Scholar
  29. 29.
    Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat Bot 82:222–237CrossRefGoogle Scholar
  30. 30.
    Cosgrove J, Borowitzka MA (2011) Chlorophyll fluorescence terminology: an introduction. In: Suggett DJ, Prášil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences, methods and developments. Developments in applied phycology, vol 4. Springer SBM, Dordrecht, pp 1–17Google Scholar
  31. 31.
    Terada R, Inoue S, Nishihara GN (2013) The effect of light and temperature on the growth and photosynthesis of Gracilariopsis chorda (Gracilariales, Rhodophtya) from geographically separated locations of Japan. J Appl Phycol 25:1863–1872CrossRefGoogle Scholar
  32. 32.
    Vo TD, Nishihara GN, Shimada S, Watanabe Y, Fujimoto M, Kawaguchi S, Terada R (2014) Taxonomic identity and the effect of temperature and light on the photosynthesis of an indoor tank-cultured red alga, Agardhiella subulata, from Japan. Fish Sci 80:281–292CrossRefGoogle Scholar
  33. 33.
    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 16:303–308CrossRefGoogle Scholar
  34. 34.
    Muraoka D, Yamamoto H, Yasui H, Terada R (1998) Formation of wound tissue of Gracilaria chorda Holmes (Gracilariaceae) in culture. Bull Fac Fish Hokkaido Univ 49:31–39Google Scholar
  35. 35.
    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 49:1–11CrossRefGoogle 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 25:399–406Google Scholar
  37. 37.
    Alexandrov GA, Yamagata Y (2007) A peaked function for modeling temperature dependence of plant productivity. Ecol Model 200:189–192CrossRefGoogle Scholar
  38. 38.
    Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547CrossRefGoogle Scholar
  39. 39.
    Webb WL, Newton M, Starr D (1974) Carbon dioxide exchange of Alnus rubra: a mathematical model. Oecologia 17:281–291CrossRefGoogle Scholar
  40. 40.
    Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701Google Scholar
  41. 41.
    Henley WJ (1993) Measurement and interpretation of photosynthetic light-response curves in algae in the context of photo inhibition and diel changes. J Phycol 29:729–739CrossRefGoogle Scholar
  42. 42.
    R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at: http://www.R-project.org
  43. 43.
    Stan Development Team (2013) Stan: a C++ library for probability and sampling, version 1.3. Available at: http://mc-stan.org
  44. 44.
    Gelman A (2004) Parameterization and Bayesian modeling. J Am Stat Assoc 99:537–545CrossRefGoogle Scholar
  45. 45.
    Gelman A (2006) Prior distributions for variance parameters in hierarchical models. Bayesian Anal 1:515–533CrossRefGoogle Scholar
  46. 46.
    Dongsansuk A, Lutz C, Neuner G (2013) Effects of temperature and irradiance on quantum yield of PSII photochemistry and xanthophyll cycle in a tropical and temperate species. Photosynthetica 51:13–21CrossRefGoogle Scholar
  47. 47.
    Salvucci ME, Crafts-Brandner SJ (2004) Relationship between the heat tolerance of photosynthesis and the thermal stability of rubisco activase in plants from contrasting thermal environments. Plant Physiol 134:1460–1470PubMedCentralPubMedCrossRefGoogle Scholar
  48. 48.
    Roháček K (2002) Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40:13–29CrossRefGoogle Scholar
  49. 49.
    Yokono M, Murakami A, Akimoto S (2011) Excitation energy transfer between photosystem II and photosystem I in red algae: larger amounts of phycobilisome enhance spillover. Biochim Biophys Acta Bioenerg 1807:847–853CrossRefGoogle Scholar
  50. 50.
    Larkum AWD (2003) Light-harvesting systems in algae. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in algae. Kluwer, Dordrecht, pp 277–304CrossRefGoogle Scholar
  51. 51.
    Larkum AWD, Vesk M (2003) Algal plastids: their fine structure and properties. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in algae. Kluwer, Dordrecht, pp 11–28CrossRefGoogle Scholar
  52. 52.
    Kowalczyk N, Rappaport F, Boyen C, Wollman FA, Collen J, Joliot P (2013) Photosynthesis in Chondrus crispus: the contribution of energy spill-over in the regulation of excitonic flux. Biochim Biophys Acta Bioenerg 1827:834–842CrossRefGoogle Scholar
  53. 53.
    Zhang T, Li J, Ma F, Lu Q, Shen Z, Zhu J (2014) Study of photosynthetic characteristics of the Pyropia yezoensis thallus during the cultivation process. J Appl Phycol 26:859–865Google Scholar
  54. 54.
    Pang SJ, Zhang ZH, Zhao HJ, Sun JZ (2007) Cultivation of the brown alga Hizikia fusiformis (Harvey) Okamura: stress resistance of artificially raised young seedlings revealed by chlorophyll fluorescence measurement. J Appl Phycol 19:557–565CrossRefGoogle Scholar
  55. 55.
    Domínguez-Álvarez S, Rico JM, Gil-Rodríguez MC (2011) Photosynthetic response and zonation of three species of Gelidiales from Tenerife, Canary Islands. An Jard Bot Madrid 68:117–124CrossRefGoogle Scholar
  56. 56.
    Takase T, Tanaka Y, Kurokawa M, Nohara S (2008) ISOYAKE (Barren Sea) of Gelidium bed in Hachijo-jima Island, Izu Islands. Nippon Suisan Gakkaishi 74:889–891CrossRefGoogle Scholar
  57. 57.
    Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trend Plant Sci 8:343–351CrossRefGoogle Scholar

Copyright information

© The Japanese Society of Fisheries Science 2014

Authors and Affiliations

  • Midori Fujimoto
    • 1
  • Gregory N. Nishihara
    • 2
  • Ryuta Terada
    • 1
    Email author
  1. 1.Faculty of FisheriesKagoshima UniversityKagoshimaJapan
  2. 2.Institute for East China Sea Research, Graduate School of Fisheries Science and Environmental StudiesNagasaki UniversityNagasakiJapan

Personalised recommendations