Effect of photosynthetically active radiation and temperature on the photosynthesis of two heteromorphic life history stages of a temperate edible brown alga, Cladosiphon umezakii (Chordariaceae, Ectocarpales), from Japan

Abstract

The effect of photosynthetically active radiation (PAR) and temperature on the photosynthesis of a temperate Japanese edible brown alga, Cladosiphon umezakii (Chordariaceae, Ectocarpales), from Honshu Island, Japan, was determined in the heteromorphic life history stages (macroscopic and microscopic) by using pulse-amplitude modulation (PAM) fluorometry and optical dissolved oxygen sensors. The microscopic stage is well-adapted to relatively low PAR environment, as revealed by its lower maximum net photosynthesis (NPmax), saturation (Ek), and compensation PAR (Ec), and higher value of the initial slope (α) compared to the macroscopic stage. Both stages share similar temperature optima (\( {T}_{opt}^{GP} \) 15.9–25.8 °C for macroscopic stage, 12.6–27.4 °C for microscopic stage), suggesting the possible occurrence of both generations in their habitats throughout the year. While these optimum temperatures are within the range of seawater temperature in the distribution of this species, they are close to the physiological limit of thermal inhibition. Continuous exposures (6 h) to 200 (low) and 1000 (high) μmol photons m−2 s−1 at 8, 16, and 28 °C revealed greater declines in effective quantum yields of photosystem II (ΦPSII) in the microscopic stage, confirming its low PAR adaptation. Low temperature-induced photoinhibition was likewise observed in both stages. Existing farming methods for Japanese Cladosiphon (especially for subtropical Cladosiphon okamuranus from Ryukyu Islands, Japan) may need to be modified to meet the optimum requirements of C. umezakii in the temperate region of Japan.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Aguirre von Wobeser E, Figueroa F, Cabello-Pasini A (2001) Photosynthesis and growth of the red and green morphotypes of Kappaphycus alvarezii (Rhodophyta) from the Philippines. Mar Biol 138:679–686

    Article  CAS  Google Scholar 

  2. Ajisaka T, Kim SH, Uwai S, Kawai H (2007) Cladosiphon umezakii sp. nov. (Ectocarpales, Phaeophyceae) from Japan. Phycol Res 55:193–202

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  4. Allakhverdiev SI, Kreslavski V, Klimov V, Los D, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541–550

    Article  CAS  PubMed  Google Scholar 

  5. Altamirano M, Murakami A, Kawai H (2004) High light stress in the kelp Ecklonia cava. Aquat Bot 79:125–135

    Article  Google Scholar 

  6. Beer S, Björk M, Beardall J (2014) Photosynthesis in the marine environment. Wiley, Iowa

    Google Scholar 

  7. Bessho K, Iwasa Y (2010) Optimal seasonal schedules and the relative dominance of heteromorphic and isomorphic life cycles in macroalgae. J Theor Biol 267:201–212

    Article  PubMed  Google Scholar 

  8. Bolton JJ, Lüning K (1983) Optimal growth and maximal survival temperatures of Atlantic Laminaria species (Phaeophyta) in culture. Mar Biol 66:89–94

    Article  Google Scholar 

  9. Borlongan IA, Gerung GS, Kawaguchi S, Nishihara GN, Terada R (2016) Thermal and PAR effects on the photosynthesis of Eucheuma denticulatum and Kappaphycus striatus (so-called Sacol strain) cultivated in shallow bottom of Bali, Indonesia. J Appl Phycol 29:395–404

    Article  CAS  Google Scholar 

  10. Borlongan IA, Nishihara GN, Shimada S, Terada R (2017) Photosynthetic performance of the red alga Solieria pacifica (Solieriaceae) from two different depths in the sublittoral waters of Kagoshima, Japan. J Appl Phycol 29:3077–3088

    Article  CAS  Google Scholar 

  11. Borlongan IA, Matsumoto K, Nakazaki Y, Shimada N, Kozono J, Nishihara GN, Shimada S, Watanabe Y, Terada R (2018) Photosynthetic activity of two life history stages of Costaria costata (Laminariales, Phaeophyceae) in response to PAR and temperature gradient. Phycologia 57:159–168

    Article  Google Scholar 

  12. Colombo-Pallotta MF, Rodríguez-Román A, Iglesias-Prieto R (2010) Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs 29:899–907

    Article  Google Scholar 

  13. 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. Springer, Dordrecht, pp 1–17

    Google Scholar 

  14. Dan A, Yoshimi K, Yamamoto K (2003) Ecology of Cladosiphon umezakii on the Pacific coast of Tokushima Prefecture in Japan. Bull Tokushima Pref Fish Res Ins 2:27–33 (in Japanese with English Abstract)

    Google Scholar 

  15. Davison IR (1987) Adaptation of photosynthesis in Laminaria saccharina (Phaeophyta) to changes in growth temperature. J Phycol 23:273–283

    Article  Google Scholar 

  16. Delebecq G, Davoult D, Menu D, Janquin MA, Migné A, Dauvin JC, Gevaert F (2011) In situ photosynthetic performance of Laminaria digitata (Phaeophyceae) during spring tides in Northern Brittany. Cah Biol Mar 52:405–414

    Google Scholar 

  17. Delebecq G, Davoult D, Menu D, Janquin MA, Migné A, Dauvin JC, Gevaert F (2016) Photosynthetic response to light and temperature in Laminaria digitata gametophytes from two French populations. Eur J Phycol 51:71–82

    Article  CAS  Google Scholar 

  18. Eggert A (2012) Seaweed responses to temperature. In: Wiencke C, Bischof K (eds) Seaweed biology. Springer, Berlin, pp 47–66

    Google Scholar 

  19. Eggert A, Burger EM, Breeman A (2003) Ecotypic differentiation in thermal traits in the tropical to warm-temperate green macrophyte Valonia utricularis. Bot Mar 46:69–81

    Article  Google Scholar 

  20. Faraway JJ (2016) Extending the linear model with R, 2nd edn. CRC Press, Boca Raton

    Google Scholar 

  21. Fukumoto R, Borlongan IA, Nishihara GN, Endo H, Terada R (2018) The photosynthetic responses to PAR and temperature including chilling-light stress on the heteromorphic life history stages of a brown alga, Cladosiphon okamuranus (Chordariaceae) from Ryukyu Islands, Japan. Phycol Res 66:209–217

    Article  CAS  Google Scholar 

  22. 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 

  23. Gévaert F, Creach A, Davoult D, Holl AC, Seuront L, Lemoine Y (2002) Photo-inhibition and seasonal photosynthetic performance of the seaweed Laminaria saccharina during a simulated tidal cycle: chlorophyll fluorescence measurements and pigment analysis. Plant Cell Environ 25:859–872

    Article  Google Scholar 

  24. Gómez I, Wulff A, Roleda M, Huovinen P, Karsten U, Quartino ML, Dunton K, Wiencke C (2011) Light and temperature demands of marine benthic microalgae and seaweeds in polar regions. In: Wiencke C (ed) Biology of polar benthic algae. Walter de Gruyter, Berlin, pp 195–220

    Google Scholar 

  25. Hanelt D, Wiencke C, Karsten U (1997a) Photoinhibition and recovery after high light stress in different development and life-history stages of Laminaria saccharina (Phaeophyta). J Phycol 33:387–395

    Article  Google Scholar 

  26. Hanelt D, Wiencke C, Karsten U (1997b) Effects of high light stress on photosynthesis of polar macroalgae in relation to depth distribution. Mar Ecol Prog Ser 149:255–266

    Article  CAS  Google Scholar 

  27. Heinrich S, Valentin K, Frickenhaus S, Wiencke C (2015) Temperature and light interactively modulate gene expression in Saccharina latissima (Phaeophyceae). J Phycol 51:93–108

    Article  CAS  PubMed  Google Scholar 

  28. 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 

  29. Japan Oceanographic Data Center (2018) JODC data on-line service system. http://jdoss1.jodc.go.jp/vpage/coastal_j.html (accessed on 8 Mar 2018; in Japanese)

  30. 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 

  31. Kawai H, Hanyuda T, Kim SH, Ichikawa Y, Uwai S, Peters AF (2016) Cladosiphon takenoensis sp. nov. (Ectocarpales s.l., Phaeophyceae) from Japan. Phycol Res 64:212–218

    Article  CAS  Google Scholar 

  32. Moromizato S, Masuda A, Horaguchi K, Murakami K (2005) Technical change to the seedling collection and cultivation of edible brown alga, Okinawa-Mozuku, Cladosiphon okamuranus. Eco-Eng 17:23–26 (in Japanese with English Abstract)

    Google Scholar 

  33. Navarro NP, Huovinen P, Gómez I (2016) Stress tolerance of Antarctic macroalgae in the early life stages. Rev Chil de Hist Nat 89:5

    Article  Google Scholar 

  34. Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701

    Google Scholar 

  35. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  36. R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna ISBN 3-900051-07-0, http://www.R-project.org

  37. Rmiki NE, Schoefs B, Lemoine Y (1998) Carotenoids and stress in higher plants and algae. In: Pessarakli M (ed) Handbook of plant and crop stress. Marcel Dekker, New York, pp 465–482

    Google Scholar 

  38. Roleda MY (2009) Photosynthetic response of Arctic kelp zoospores exposed to radiation and thermal stress. Photobiol Sci 8:1302–1312

    Article  CAS  Google Scholar 

  39. Roleda MY (2016) Stress physiology and reproductive phenology of Arctic endemic kelp Laminaria solidungula J. Agardh. Polar Biol 39:1967–1977

    Article  Google Scholar 

  40. Roleda MY, Wiencke C, Hanelt D, van de Poll WH, Gruber A (2005) Sensitivity of Laminariales zoospores from Helgoland (North Sea) to ultraviolet and photosynthetically active radiation: implications for depth distribution and seasonal reproduction. Plant Cell Environ 28:466–479

    Article  Google Scholar 

  41. Saonsón M, Marín MJ, Reyes J (2006) Vegetative and reproductive morphology of Cladosiphon contortus, C. occidentalis and C. cymodoceae sp. nov. (Ectocarpales, Phaeophyceae) from the Canary Islands. Phycologia 45:529–545

    Article  Google Scholar 

  42. Schoenwaelder MEA, Wiencke C, Clayton MN, Glombitza KW (2003) The effect of elevated UV radiation on Fucus spp. (Fucales, Phaeophyta) zygote and embryo development. Plant Biol 5:366–377

    Article  Google Scholar 

  43. Schubert N, Colombo-Pallota MF, Enríquez S (2015) Leaf and canopy scale characterization of the photoprotective response to high-light stress of the seagrass Thalassia testudinum. Limnol Oceanol 60:286–302

    Article  CAS  Google Scholar 

  44. Shinmura I (1976) Studies on the cultivation of an edible brown alga, Cladosiphon okamuranus – V. conjunction of gamete and development of zygote. Bull Jap Soc Sci Fish 42:21–28 (in Japanese with English abstract)

    Article  Google Scholar 

  45. Shinmura I (1977) Life history of Cladosiphon okamuranus Tokida from southern Japan. Bull Jpn Soc Phycol 25:333–340 (in Japanese with English Abstract)

    Google Scholar 

  46. Shinmura I, Yamanaka K (1974a) Studies on the cultivation of an edible brown alga, Cladosiphon okamuranus—I. The season for seeding of zoospore and its growth. Bull Jpn Soc Sci Fish 40:895–902 (in Japanese with English Abstract)

    Article  Google Scholar 

  47. Shinmura I, Yamanaka K (1974b) Studies on the cultivation of an edible brown alga, Cladosiphon okamuranus—II. Field culture experiments with a culture-net. Bull Jpn Soc Sci Fish 40:1133–1138 (in Japanese with English Abstract)

    Article  Google Scholar 

  48. Stan Development Team (2017) RStan: the R interface to Stan. R package version 2.17.3. http://mc-stan.org

  49. Sudo Y (2012) Cladosiphon okamuranus. In: Watanabe MM et al (eds) Handbook of algae. Their diversity and utilization. NTS, Tokyo, pp 575–579 in Japanese

    Google Scholar 

  50. Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182

    Article  CAS  PubMed  Google Scholar 

  51. Tala F, Edding M, Vásquez J (2004) Aspects of the reproductive phenology of Lessonia trabeculata (Laminariales: Phaeophyceae) from three populations in northern Chile. N Z J Mar Freshw Res 38:255–266

    Article  Google Scholar 

  52. Tala F, Penna-Díaz A, Luna-Jorquera G, Rothäusler E, Thiel M (2017) Daily and seasonal changes of photobiological responses in floating bull kelp Durvillaea antarctica (Chamisso) Hariot (Fucales: Phaeophyceae). Phycologia 56:271–283

    Article  CAS  Google Scholar 

  53. Terada R, Matsumoto K, Borlongan IA, Watanabe Y, Nishihara GN, Endo H, Shimada S (2018) The combined effects of PAR and temperature including the chilling-light stress on the photosynthesis of a temperate brown alga, Sargassum patens (Fucales), based on field and laboratory measurements. J Appl Phycol 61:1893–1904

    Article  CAS  Google Scholar 

  54. Thornley JHM, Johnson IR (2000) Plant and crop modelling: a mathematical approach to plant and crop physiology. Blackburn Press, Caldwell, p 669

    Google Scholar 

  55. Titlyanov EA, Titlyanova TV (2012) Marine plants of the Asian Pacific region countries, their use and cultivation. Dalnauka and A.V. Zhirmunsky Institute of Marine Biology, Vladivostok, p 376

    Google Scholar 

  56. Tokida J (1942) Phycological observations, V. Trans Sapporo Nat Hist Soc 17:82–95

    Google Scholar 

  57. tom Dieck I (1992) North Pacific and North Atlantic digitate Laminaria species (Phaeophyta): hybridization experiments and temperature responses. Phycologia 31:147–163

    Article  Google Scholar 

  58. Toma T (1993) Cultivation of the brown alga, Cladosiphon okamuranus “Okinawa-mozuku”. In: Ohno M, Critchley AT (eds) Seaweed cultivation and marine ranching. Japan International Cooperation Agency, Yokosuka, pp 51–56

    Google Scholar 

  59. Vásquez-Elizondo RM, Enríquez S (2016) Coralline algal physiology is more adversely affected by elevated temperature than reduced pH. Sci Rep 6:19030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Véliz K, Edding M, Tala F, Gomez I (2006) Effects of ultraviolet radiation on different life cycle stages of the south Pacific kelps Lessonia nigrescens and L. trabeculata (Laminariales, Phaeophyceae). Mar Biol 149:1015–1024

    Article  CAS  Google Scholar 

  61. 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 62:187–196

    Article  CAS  Google Scholar 

  62. Watanabe Y, Yamada H, Mine Y, Kawamura Y, Nishihara GN, Terada R (2016) Photosynthetic responses of Pyropia yezoensis f. narawaensis (Bangiales, Rhodophyta) to a thermal and PAR gradient vary with the life-history stage. Phycologia 55:665–672

    Article  CAS  Google Scholar 

  63. Webb WL, Newton M, Starr D (1974) Carbon dioxide exchange of Alnus rubra: a mathematical model. Oecologia 17:281–291

    Article  PubMed  Google Scholar 

  64. Wiencke C, Amsler CD (2012) Seaweeds and their communities in polar regions. In: Wiencke C, Bischof K (eds) Seaweed biology, novel insights into ecophysiology, ecology and utilization. Springer, Berlin, pp 265–291

    Google Scholar 

  65. Wiencke C, Lüder UH, Roleda MY (2007) Impact of ultraviolet radiation on physiology and development of zoospores of the brown alga Alaria esculenta from Spitsbergen. Physiol Plant 130:601–612

    Article  CAS  Google Scholar 

  66. Yoshimi K, Hirosawa A, Yamamoto K (2005) Seed production of the brown alga Cladosiphon sp. using tissue culture for artificial seeding (short paper). Bull Tokushima Pref Fish Res Ins 4:43–45 (in Japanese)

    Google Scholar 

  67. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GA (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Google Scholar 

Download references

Acknowledgements

We thank Prof. Hiroshi Kawai, Kobe University Research Center for Inland Seas, for his kind arrangement and support during the field survey. We also note that the field survey was conducted in collaboration with the nation-wide long-term monitoring survey for seaweed communities (Monitoring Site 1000) of the Japanese Ministry of the Environment. All authors have provided consent.

Funding

This research was supported in part by the Grant-in-Aid for Scientific Research (#26241027 and #16H02939) from Japan Society for the Promotion of Science (JSPS) and the Japanese Ministry of Education, Culture, Sports, Science and Technology (MEXT).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ryuta Terada.

Electronic supplementary material

ESM 1

(DOCX 32 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Fukumoto, R., Borlongan, I.A., Nishihara, G.N. et al. Effect of photosynthetically active radiation and temperature on the photosynthesis of two heteromorphic life history stages of a temperate edible brown alga, Cladosiphon umezakii (Chordariaceae, Ectocarpales), from Japan. J Appl Phycol 31, 1259–1270 (2019). https://doi.org/10.1007/s10811-018-1655-3

Download citation

Keywords

  • Algae
  • Cladosiphon
  • Heteromorphic life history
  • Mozuku
  • Photosynthesis
  • Pulse-amplitude modulation (PAM)-chlorophyll fluorometry