The effect of irradiance and temperature on the photosynthesis of an agarophyte, Gelidiella acerosa (Gelidiales, Rhodophyta), from Krabi, Thailand

Abstract

The effect of irradiance and temperature on the photosynthesis of an agarophyte from Thailand, Gelidiella acerosa (Gelidiales, Rhodophyta), was determined using dissolved oxygen sensors and pulse-amplitude modulated fluorometry (PAM). A model of the net photosynthesis–irradiance (PE) curve at 28 °C revealed that the saturation and compensation irradiances were 83 (95 % Bayesian credible interval (BCI), 52–128) μmol photons m−2 s−1 and 37 (BCI, 29–45) μmol photons m−2 s−1, respectively. Gross photosynthesis and dark respiration were also determined over a range of temperatures (16–40 °C), revealing that the gross photosynthetic rate was highest at 18.4 (BCI, 15.9–20.8) mg O2 gww −1 min−1 at 29.2 (BCI, 26.8–32.1) °C. Dark respiration rate could be fitted to a second-order polynomial regression (P < 0.01) over the range of the experimental temperatures, and the magnitudes of the rates ranged from 0.49 to 0.93 mg O2 gww −1 min−1 °C−1. The highest value of the maximum effective quantum yield (ΦPSII at 0 μmol photons m−2 s−1) occurred at 27.7 (BCI, 26.5–28.9) °C and was 0.57 (BCI, 0.55–0.58), and the values of ΦPSII decreased above and below 27.7 °C. Although this species is considered to be well-adapted to the current seawater temperatures of the region, the results of the experiments also suggest that they are likely close to the limiting temperature conditions.

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References

  1. Abbott IA (1999) Marine red algae of the Hawaiian Islands. Bishop Museum Press, Honolulu, 477 pp

    Google Scholar 

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

    Article  Google Scholar 

  3. Armisen R, Galatas F (1987) Production, properties and uses of agar. In McHugh DJ (ed) Production and Utilization of Products from Commercial Seaweeds. FAO Fish. Tech. Pap. 288: 1-57

  4. Atkin OK, Tjoelker MG (2003) Thermal acclimation and the dynamic response of plant respiration to temperature. Trends Plant Sci 8:343–351

    Article  CAS  PubMed  Google Scholar 

  5. Bell EC (1993) Photosynthetic response to temperature and desiccation of the intertidal alga Mastocarpus papillatus. Mar Biol 117:337–346

    Article  Google Scholar 

  6. Brown BE, Dunne RP, Chansang H (1996) Coral bleaching relative to elevated seawater temperature in the Andaman Sea (Indian Ocean) over the last 50 years. Coral Reefs 15:151–152

    Article  Google Scholar 

  7. Bunsom C, Prathep A (2012) Effect of salinity, light intensity and sediment on growth, pigments, agar production and reproduction in Gracilaria tenuistipitata from Songkhla Lagoon in Thailand. Phycol Res 60:169–178

    Article  Google Scholar 

  8. Chennubhotla VSK, Kalimuthu S, Najmuddin M, Panigrahy R, Selvaraj M (1986) Changes in growth and phycocolloid content of Gelidiella acerosa and Gracilaria edulis. Seaweed Res Util 9:45–48

    Google Scholar 

  9. Chihara M, Kamura S (1963) On the germination of tetraspores of Gelidiella acerosa. Phycologia 3:69–74

    Article  Google Scholar 

  10. Coppejans E, Prathep A, Leliaert F, Lewmanomont K, De Clerck O (2011) Seaweeds of Mu Ko Tha Lae Tai (SE Thailand). Methodologies and field guide to the dominant species. Biodiversity Research and Training Program (BRT), Bangkok, 274 pp

    Google Scholar 

  11. Davison IR, Perason GA (1996) Stress tolerance in intertidal seaweeds. J Phycol 32:197–211

    Article  Google Scholar 

  12. R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org

  13. 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 51:13–21

    Article  CAS  Google Scholar 

  14. Dring MJ, Brown FA (1982) Photosynthesis of intertidal brown algae during and after periods of emersion: a renewed search for physiological causes of zonation. Mar Ecol Prog Ser 8:301–308

    Article  Google Scholar 

  15. Edwards MS, Kim KY (2010) Diurnal variation in relative photosynthetic performance in giant kelp Macrocystis pyrifera (Phaeophyceae, Laminariales) at different depths as estimated using PAM fluorometry. Aquat Bot 92:119–128

    Article  CAS  Google Scholar 

  16. Edwards P, Tam DM (1984) The potential for Gracilaria farming in Thailand. Hydrobiologia 116/117:246–248

    Article  Google Scholar 

  17. Fujimoto M, Nishihara GN, Terada R (2014a) The effect of irradiance and temperature on the photosynthesis of two agarophytes Gelidium elegans and Pterocladiella tenuis (Gelidiales) from Kagoshima, Japan. Fish Sci 80:695–703

    Article  CAS  Google Scholar 

  18. Fujimoto M, Nitta K, Nishihara GN, Terada R (2014b) Phenology, irradiance and temperature characteristics of a freshwater red alga, Nemalionopsis tortuosa (Thoreales), from Kagoshima, southern Japan. Phycol Res 62:77–85

    Article  CAS  Google Scholar 

  19. Ganzon-Fortes ET (1994) Gelidiella. In: Akatsuka I (ed) Biology of economic algae. SPB Academic Publishing, Hague, pp 149–184

    Google Scholar 

  20. Ganzon-Fortes ET (1997a) Diurnal and diel patterns in the photosynthetic performance of the agarophyte Gelidiella acerosa. Bot Mar 40:93–100

    Article  CAS  Google Scholar 

  21. Ganzon-Fortes ET (1997b) Influence of tidal location on morphology, photosynthesis and pigments of the agarophyte, Gelidiella acerosa, from Northern Philippines. J Appl Phycol 9:525–532

    CAS  Google Scholar 

  22. Ganzon-Fortes ET (1999) Photosynthetic and respiratory responses of the agarophyte Gelidiella acerosa collected from tidepool, intertidal and subtidal habitats. Hydrobiologia 398/399:321–328

    Article  Google Scholar 

  23. Gelman A (2004) Parameterization and Bayesian modeling. J Am Stat Assoc 99:537–545

    Article  Google Scholar 

  24. Gelman A (2006) Prior distributions for variance parameters in hierarchical models. Bayesian Anal 1:515–533

    Article  Google Scholar 

  25. Henley WJ (1993) Measurement and interpretation of photosynthetic light-response curves in algae in the context of photo inhibition and diel changes. J Phycol 29:729–39

    Article  Google Scholar 

  26. 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 

  27. 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 1827:834–842

    Article  CAS  Google Scholar 

  28. Kübler JE, Davison IR (1993) High-temperature tolerance of photosynthesis in the red alga Chondrus crispus. Mar Biol 117:325–335

    Article  Google Scholar 

  29. Larkum AWD (2003) Light-harvesting systems in algae. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in algae. Kluwer, Dordrecht, pp 277–304

    Google Scholar 

  30. 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 11–28

    Google Scholar 

  31. Lewmanomont K, Ogawa H (1995) Common seaweeds and seagrasses of Thailand. Faculty of Fisheries, Kasetsart University, Bangkok, 163 p

    Google Scholar 

  32. 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

    Article  CAS  Google Scholar 

  33. Lin SM, Freshwater DW (2008) The red algal genus Gelidiella (Gelidiales, Rhodophyta) from Taiwan, including Gelidiella fanii sp. nov. Phycologia 47:168–176

    Article  Google Scholar 

  34. Lüning K (1984) Temperature tolerance and biogeography of seaweeds: the marine algal flora of Helgoland (North Sea) as an example. Helgol Meeresunters 38:305–317

    Article  Google Scholar 

  35. McHugh DJ (1991) Worldwide distribution of commercial resources of seaweeds inc1uding Gelidium. Hydrobiologia 221:12–29

    Article  Google Scholar 

  36. 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 49:31–39

    Google Scholar 

  37. 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 

  38. 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 1–14

    Google Scholar 

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

    Google Scholar 

  40. Praiboon J, Chirapart A, Akakabe Y, Bhumibhamond B, Kajiwara T (2006) Physical and chemical characterization of agar polysaccharides extracted from the Thai and Japanese species of Gracilaria. Sci Asia 32:11–17

    Article  Google Scholar 

  41. Prathep A (2005) Spatial and temporal variations in diversity and percentage cover of macroalgae at Sirinart Marine National Park, Phuket Province, Thailand. Sci Asia 31:225–233

    Article  Google Scholar 

  42. Prathep A, Wichachucherd B, Thongroy P (2007) Spatial and temporal variation in density and thallus morphology of Turbinaria ornata in Thailand. Aquat Bot 86:132–138

    Article  Google Scholar 

  43. Prathep A, Lewmanomont K, Buapet P (2009) Effects of wave exposure on population and reproductive phenology of an algal turf, Gelidium pusillum (Gelidales, Rhodophyta), Songkhla, Thailand. Aquat Bot 90:179–183

    Article  Google Scholar 

  44. Rao PS, Mehta VB (1973) Physiological ecology of Gelidiella acerosa (Forsskal) Feldmann et Hamel. J Phycol 9:333–335

    CAS  Google Scholar 

  45. Roháček K (2002) Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40:13–29

    Article  Google Scholar 

  46. Roleda MY, Montaño NE, Ganzon-Fortes ET, Villanueva RD (1997a) Acetic acid pretreatment in agar extraction of Philippine Gelidiella acerosa (Forsskaal) Feldmann et Hamel (Rhodophyta, Gelidiales). Bot Mar 40:63–70

    CAS  Google Scholar 

  47. Roleda MY, Ganzon-Fortes ET, Montaño NE, de los Reyes FN (1997b) Temporal variation in the biomass, quantity and quality of agar from Gelidiella acerosa (Forsskål) Feldmann et Hamel (Rhodophyta: Gelidiales) from Cape Bolinao, NW Philippines. Bot Mar 40:487–496

    Google Scholar 

  48. Salvucci M, 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 134:1460–1470

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. Santelices B, Stewart JG (1985) Pacific species of Gelidium Lamouroux and other Gelidiales (Rhodophyta), with keys and descriptions to the common or economically important species. In: Abbott IA, Norris JN (eds) Taxonomy of economic seaweds with reference to some Pacific and Caribbean species. California Sea Grant College Program, La Jolla, pp 17–31

    Google Scholar 

  50. Schagerl M, Möstl M (2011) Drought stress, rain and recovery of the intertidal seaweed Fucus spiralis. Mar Biol 158:2471–2479

    Article  Google Scholar 

  51. 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

    Article  CAS  PubMed  Google Scholar 

  52. 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 

  53. Smith CM, Berry JA (1986) Recovery of photosynthesis after exposure of intertidal algae to osmotic and temperature stresses: comparative studies of species with differing distributional limits. Oecologia 70:6–12

    Article  Google Scholar 

  54. Stan Development Team (2013) Stan: A C++ Library for Probability and Sampling, Version 1.3. URL: http://mc-stan.org

  55. Tanzil JTI, Brown BE, Tudhope AW, Dunne RP (2009) Decline in skeletal growth of the coral Porites lutea from the Andaman Sea, South Thailand between 1984 and 2005. Coral Reefs 28:519–528

    Article  Google Scholar 

  56. 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 25:1863–1872

    Article  CAS  Google Scholar 

  57. Thomas PC, Rao KR, Subbaramaiah K (1975) Changes in the natural growth of Gelidiella acerosa (Forskal) Feldmann et Hamel in an exploited population. Bot Mar 18:241–243

    Article  Google Scholar 

  58. Tsutsui I, Hamano K, Aue-umneoy D, Songphatkaew J, Srisapoome P, Ruangsomboon S, Klomkling S, Ganmanee M, Taveekijararn P, Maeno Y (2012) Common underwater plants in coastal areas of Thailand. International Agriculture Series No. 21. Japan International Research Center for Agricultural Studies, Tsukuba, 171 pp

    Google Scholar 

  59. Villanueva RD, Montaño NE, Romero JB, Aliganga AKA, Enriquez EP (1999) Seasonal variations in the yield, gelling properties, and chemical composition of agars from Gracilaria eucheumoides and Gelidiella acerosa (Rhodophyta) from the Philippines. Bot Mar 42:175–182

    Article  CAS  Google Scholar 

  60. 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. 80:281–292

  61. Watanabe Y, Nishihara GN, Tokunaga S, Terada R (2014a) 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

  62. Watanabe Y, Nishihara GN, Tokunaga S, Terada R (2014b) 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

    PubMed Central  PubMed  Google Scholar 

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

    Article  Google Scholar 

  64. 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 1807:847–853

    Article  CAS  Google Scholar 

  65. Zemke-White WL, Ohno M (1999) World seaweed utilisation: an end-of-century summary. J Appl Phycol 11:369–376

    Article  Google Scholar 

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Acknowledgments

We express our gratitude to Khanjanapaj Lewmanomont, Eric Coppejans and Ken-ichi Hayashizaki, for their valuable suggestions at the field survey in Krabi, Thailand. We also thank Jaruwan Mayakun, Anuchit Darakrai, Supattra Pongparadon, Ekkalak Ratanachot, and Takashi Tsunoda for their kind assistances to complete the field survey. This research was sponsored in part by a JSPS-Asian CORE Program in the Atmosphere and Ocean Research Institute, the University of Tokyo (AP and RT), and by a Grant-in-Aid for Scientific Research (nos. 22510033, 25340012, and 25450260) from the Japanese Ministry of Education, Culture, Sport and Technology (RT and GNN); partially funded by Plant Genetic Conservation Project Under the Royal Initiation of Her Royal Highness Princess Maha Chakri Sirindhorn (AP).

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Correspondence to Ryuta Terada.

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Fujimoto, M., Nishihara, G.N., Prathep, A. et al. The effect of irradiance and temperature on the photosynthesis of an agarophyte, Gelidiella acerosa (Gelidiales, Rhodophyta), from Krabi, Thailand. J Appl Phycol 27, 1235–1242 (2015). https://doi.org/10.1007/s10811-014-0409-0

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Keywords

  • Agarophyte
  • Algae
  • Gelidiella acerosa
  • Photosynthesis
  • Pulse amplitude modulation (PAM)-chlorophyll fluorometry
  • Temperature tolerance