Journal of Oceanography

, Volume 72, Issue 5, pp 761–776 | Cite as

Variation of the photosynthetic electron transfer rate and electron requirement for daily net carbon fixation in Ariake Bay, Japan

  • Y. Zhu
  • J. Ishizaka
  • S. C. Tripathy
  • S. Wang
  • Y. Mino
  • T. Matsuno
  • D. J. Suggett
Original Article

Abstract

Fast repetition rate fluorometry (FRRf) provides a potential means to examine marine primary productivity; however, FRRf-based productivity estimations require knowledge of the electron requirement (K) for carbon (C) uptake (K C) to scale an electron transfer rate (ETR) to the CO2 uptake rate. Most previous studies have derived K C from parallel measurements of ETR and CO2 uptake over relatively short incubations, with few from longer-term daily-integrated periods. Here we determined K C by comparing depth-specific, daily ETRs and CO2-uptake rates obtained from 24-h on-deck incubation experiments undertaken on seven cruises in Ariake Bay, Japan, from 2008 to 2010. The purpose of this study was to determine the extent of variability of K C and to what extent this variability could be reconciled with the prevailing environmental conditions and ultimately to develop a method for determining net primary productivity (NPP) based on FRRf measurements. Both daily ETR and K C of the upper layer varied considerably, from 0.5 to 115.7 mmol e mg Chl-a −1 day−1 and 4.1–26.6 mol e (mol C)−1, respectively, throughout the entire data set. Multivariate analysis revealed a strong correlation between daily photosynthetically active radiation (PAR) and K C (r 2 = 0.94). A simple PAR-dependent relationship derived from the data set was used for generating K C, and this relationship was validated by comparing the FRRf-predicted NPP with the 13C uptake measured in 2007. These new observations demonstrate the potential application of FRRf for estimating regional NPP from ETR.

Keywords

FRR fluorometry Primary productivity ETR Quantum requirement for carbon fixation 13C-uptake 

Notes

Acknowledgments

We wish to thank the captain, officers and crew of T/V-Kakuyo Maru for their admirable assistance during onboard sampling and measurements. We also thank Drs. W. Cheah, J.I. Goes and H. do R. Gomes and two reviewers for helping to improve this manuscript. This research was supported by the Global Observation Mission-Climate (GCOM-C) Project of the Japan Aerospace Exploration Agency. The contribution by D.J. Suggett was supported by an Australian Research Council Future Fellowship (FT130100202).

References

  1. Behrenfeld MJ, Falkowski PG (1997) Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol Oceanogr 42:1–20CrossRefGoogle Scholar
  2. Behrenfeld MJ, Kolber ZS (1999) Widespread iron limitation of phytoplankton in the South Pacific Ocean. Science 283:840–843CrossRefGoogle Scholar
  3. Brading P, Warner ME, Smith DJ, Suggett DJ (2013) Contrasting modes of inorganic carbon acquisition amongst Symbiodinium (Dinophyceae) phylotypes. New Phytol 200:432–442CrossRefGoogle Scholar
  4. Cardol P, Forti G, Finazzi G (2011) Regulation of electron transport in microalgae. BBA-Bioenergetics 1807:912–918CrossRefGoogle Scholar
  5. Cheah W, McMinn A, Griffiths FB, Westwood KJ, Wright SW et al (2011) Assessing Sub-Antarctic Zone primary productivity from fast repetition rate fluorometry. Deep-Sea Res II 58:2179–2188CrossRefGoogle Scholar
  6. Corno G, Letelier RM, Abbott MR, Karl DM (2006) Assessing primary production variability in the north pacific subtropical gyre: a comparison of fast repetition rate fluorometry and 14C measurements. J Phycol 42:51–60CrossRefGoogle Scholar
  7. Davison IR (1991) Environmental effects on algal photosynthesis: temperature. J Phycol 27(2–8):1991. doi: 10.1111/j0022-3646.00002.x Google Scholar
  8. Debes H, Gaard E, Hansen B (2008) Primary production on the Faroe shelf: temporal variability and environmental influences. J Mar Syst 74:686–697CrossRefGoogle Scholar
  9. Fujiki T, Hosaka T, Kimoto H, Ishimaru T, Saino T (2008) In situ observation of phytoplankton productivity by an underwater profiling buoy system: use of fast repetition rate fluorometry. Mar Ecol Prog Ser 353:81–88CrossRefGoogle Scholar
  10. Halsey KH, O’Malley RT, Graff JR, Milligan AJ, Behrenfeld MJ (2013) A common partitioning strategy for photosynthetic products in evolutionarily distinct phytoplankton species. New Phytol 198:1030–1038CrossRefGoogle Scholar
  11. Hama T, Miyazaki T, Ogawa Y, Iwakuma T, Takahashi M et al (1983) Measurement of photosynthetic production of a marine phytoplankton population using a stable 13C isotope. Mar Biol 73:31–36CrossRefGoogle Scholar
  12. Hancke K, Dalsgaard T, Sejr MK, Markager S, Glud RN (2015) Phytoplankton productivity in an Arctic Fjord (West Greenland): estimating electron requirements for carbon fixation and oxygen production. PLoS One 10(7):e0133275. doi: 10.1371/journal.pone.0133275 CrossRefGoogle Scholar
  13. Hirawake T, Shinmyo K, Fujiwara A, S-i Saitoh (2012) Satellite remote sensing of primary productivity in the Bering and Chukchi Seas using an absorption-based approach. ICES J Mar Sci 69:1194–1204CrossRefGoogle Scholar
  14. Ishizaka J, Kitaura Y, Touke Y, Sasaki H, Tanaka A et al (2006) Satellite detection of red tide in Ariake Sound, 1998–2001. J Oceanogr 62:37–45CrossRefGoogle Scholar
  15. Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547CrossRefGoogle Scholar
  16. Kameda T, Ishizaka J (2005) Size-fractionated primary production estimated by a two-phytoplankton community model applicable to ocean color remote sensing. J Oceanogr 61:663–672CrossRefGoogle Scholar
  17. Kishino M, Takahashi M, Okami N, Ichimura S (1985) Estimation of the spectral absorption coefficients of phytoplankton in the sea. Bull Mar Sci 37:634–642Google Scholar
  18. Kolber ZS, Falkowski PG (1993) Use of active fluorescence to estimate phytoplankton photosynthesis in situ. Limnol Oceanogr 38:1646–1665CrossRefGoogle Scholar
  19. Kolber ZS, Prášil O, Falkowski PG (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. BBA-Bioenergetics 1367:88–106CrossRefGoogle Scholar
  20. Kromkamp JC, Dijkman NA, Peene J, Simis SG, Gons HJ (2008) Estimating phytoplankton primary production in Lake IJsselmeer (The Netherlands) using variable fluorescence (PAM-FRRF) and C-uptake techniques. Eur J Phycol 43:327–344CrossRefGoogle Scholar
  21. Lavaud J, Rousseau B, Etienne AL (2004) General features of photoprotection by energy dissipation in planktonic diatoms (Bacillariophyceae). J Phycol 40:130–137CrossRefGoogle Scholar
  22. Lawrenz E, Silsbe G, Capuzzo E, Ylöstalo P, Forster RM et al (2013) Predicting the electron requirement for carbon fixation in seas and oceans. PLoS One 8(3):e58137. doi: 10.1371/journal.pone.0058137 CrossRefGoogle Scholar
  23. López-Sandoval DC, Rodríguez-Ramos T, Cermeño P, Sobrino C, Marañón E (2014) Photosynthesis and respiration in marine phytoplankton: relationship with cell size, taxonomic affiliation, and growth phase. J Exp Mar Biol Ecol 457:151–159CrossRefGoogle Scholar
  24. Mackey KR, Paytan A, Grossman AR, Bailey S (2008) A photosynthetic strategy for coping in a high-light, low-nutrient environment. Limnol Oceanogr 53:900–913CrossRefGoogle Scholar
  25. Marra JF (2009) Net and gross productivity: weighing in with 14C. Aquat Microb Ecol 56:123–131CrossRefGoogle Scholar
  26. Marra JF (2015) Ocean productivity: a personal perspective since the first Liege Colloquium. J Mar Syst 147:3–8CrossRefGoogle Scholar
  27. McDonald AE, Ivanov AG, Bode R, Maxwell DP, Rodermel SR et al (2011) Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). BBA-Bioenergetics 1807:954–967CrossRefGoogle Scholar
  28. Melrose DC, Oviatt CA, O Reilly JE, Berman MS (2006) Comparisons of fast repetition rate fluorescence estimated primary production and 14C uptake by phytoplankton. Mar Ecol Prog Ser 311:37–46CrossRefGoogle Scholar
  29. Mino Y, Matsumura S, Lirdwitayaprasit T, Fujiki T, Yanagi T et al (2014) Variations in phytoplankton photo-physiology and productivity in a dynamic eutrophic ecosystem: a fast repetition rate fluorometer-based study. J Plankton Res 36:398–411CrossRefGoogle Scholar
  30. Moore CM, Suggett DJ, Hickman AE, Kim Y-N, Tweddle JF et al (2006) Phytoplankton photoacclimation and photoadaptation in response to environmental gradients in a shelf sea. Limnol Oceanogr 51:936–949CrossRefGoogle Scholar
  31. Moore CM, Mills MM, Langlois R, Milne A, Achterberg EP et al (2008) Relative influence of nitrogen and phosphorous availability on phytoplankton physiology and productivity in the oligotrophic sub-tropical North Atlantic Ocean. Limnol Oceanogr 53:291–305CrossRefGoogle Scholar
  32. Ott T, Clarke J, Birks K, Johnson G (1999) Regulation of the photosynthetic electron transport chain. Planta 209:250–258CrossRefGoogle Scholar
  33. Oxborough K, Moore CM, Suggett DJ, Lawson T, Chan HG et al (2012) Direct estimation of functional PSII reaction center concentration and PSII electron flux on a volume basis: a new approach to the analysis of Fast Repetition Rate fluorometry (FRRf) data. Limnol Oceanogr: Methods 10:142–154CrossRefGoogle Scholar
  34. Prasil O, Kolber Z, Berry JA, Falkowski PG (1996) Cyclic electron flow around photosystem II in vivo. Photosynth Res 48:395–410CrossRefGoogle Scholar
  35. Raateoja M, Seppälä J, Kuosa H (2004) Bio-optical modelling of primary production in the SW Finnish coastal zone, Baltic Sea: fast repetition rate fluorometry in Case 2 waters. Mar Ecol Prog Ser 267:9–26CrossRefGoogle Scholar
  36. Robinson C, Suggett D, Cherukuru N, Ralph P, Doblin M (2014) Performance of fast repetition rate fluorometry based estimates of primary productivity in coastal waters. J Mar Syst 139:299–310CrossRefGoogle Scholar
  37. Saba VS, Friedrichs MAM, Antoine D, Armstrong RA, Asanuma I et al (2011) An evaluation of ocean color model estimates of marine primary productivity in coastal and pelagic regions across the globe. Biogeosciences 8:489–503CrossRefGoogle Scholar
  38. Schuback N, Schallenberg C, Duckham C, Maldonado MT, Tortell PD (2015) Interacting effects of light and iron availability on the coupling of photosynthetic electron transport and CO2-assimilation in marine phytoplankton. PLoS One 10(7):e0133235. doi: 10.1371/journal.pone.0133235 CrossRefGoogle Scholar
  39. Serôdio J, Lavaud J (2011) A model for describing the light response of the nonphotochemical quenching of chlorophyll fluorescence. Photosynth Res 108:61–76CrossRefGoogle Scholar
  40. Shibata T, Tripathy SC, Ishizaka J (2010) Phytoplankton pigment change as a photoadaptive response to light variation caused by tidal cycle in Ariake Bay, Japan. J Oceanogr 66:831–843CrossRefGoogle Scholar
  41. Silsbe GM, Oxborough K, Suggett DJ, Forster RM, Ihnken S et al (2015) Toward autonomous measurements of photosynthetic electron transport rates: an evaluation of active fluorescence-based measurements of photochemistry. Limnol Oceanogr: Methods 13:138–155CrossRefGoogle Scholar
  42. Smyth T, Pemberton K, Aiken J, Geider R (2004) A methodology to determine primary production and phytoplankton photosynthetic parameters from fast repetition rate fluorometry. J Plankton Res 26:1337–1350CrossRefGoogle Scholar
  43. Suggett DJ, Kraay G, Holligan P, Davey M, Aiken J et al (2001) Assessment of photosynthesis in a spring cyanobacterial bloom by use of a fast repetition rate fluorometer. Limnol Oceanogr 46:802–810CrossRefGoogle Scholar
  44. Suggett DJ, MacIntyre HL, Geider RJ (2004) Evaluation of biophysical and optical determinations of light absorption by photosystem II in phytoplankton. Limnol Oceanogr: Methods 2:316–332CrossRefGoogle Scholar
  45. Suggett DJ, Moore CM, Marañón E, Omachi C, Varela RA et al (2006a) Photosynthetic electron turnover in the tropical and subtropical Atlantic Ocean. Deep-Sea Res II:1573–1592Google Scholar
  46. Suggett DJ, Maberly SC, Geider RJ (2006b) Gross photosynthesis and lake community metabolism during the spring phytoplankton bloom. Limnol Oceanogr 51:2064–2076CrossRefGoogle Scholar
  47. Suggett DJ, Warner ME, Smith DJ, Davey P, Hennige S et al (2008) Photosynthesis and production of hydrogen peroxide by symbiodinium (pyrrhophyta) phylotypes with different thermal tolerances. J Phycol 44:948–956CrossRefGoogle Scholar
  48. Suggett DJ, MacIntyre HL, Kana TM, Geider RJ (2009a) Comparing electron transport with gas exchange: parameterising exchange rates between alternative photosynthetic currencies for eukaryotic phytoplankton. Aquat Microb Ecol 56:147–162CrossRefGoogle Scholar
  49. Suggett DJ, Moore CM, Hickman AE, Geider RJ (2009b) Interpretation of fast repetition rate (FRR) fluorescence: signatures of phytoplankton community structure versus physiological state. Mar Ecol Prog Ser 376:1–19CrossRefGoogle Scholar
  50. Suggett DJ, Moore MC, Geider RJ (2011) Estimating aquatic productivity from active fluorescence measurements. In: Chlorophyll a fluorescence in aquatic sciences: methods and applications, Chapter 6. Springer, pp 103–115Google Scholar
  51. Suggett DJ, Goyen S, Evenhuis C, Szabó M, Pettay DT et al (2015) Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation. New Phytol 208:370–381CrossRefGoogle Scholar
  52. Suzuki R, Ishimaru T (1990) An improved method for the determination of phytoplankton chlorophyll using N,N-dimethylformamide. J Oceanogr Soc Jpn 46:190–194CrossRefGoogle Scholar
  53. Tabata T, Hiramatsu K, Harada M (2015) Assessment of the water quality in the ariake sea using principal component analysis. J Water Resour Prot 7:41–49CrossRefGoogle Scholar
  54. Tripathy SC, Ishizaka J, Fujiki T, Shibata T, Okamura K et al (2010) Assessment of carbon- and fluorescence-based primary productivity in Ariake Bay, southwestern Japan. Estuar Coast Shelf Sci 87:163–173CrossRefGoogle Scholar
  55. Tripathy SC, Ishizaka J, Siswanto E, Shibata T, Mino Y (2012) Modification of the vertically generalized production model for the turbid waters of Ariake Bay, southwestern Japan. Estuar Coast Shelf S 97:66–77CrossRefGoogle Scholar
  56. Wang SQ, Ishizaka J, Yamaguchi H, Tripathy SC, Hayashi M et al (2014) Influence of the Changjiang River on the light absorption properties of phytoplankton from the East China Sea. Biogeosciences 11:1759–1773CrossRefGoogle Scholar

Copyright information

© The Oceanographic Society of Japan and Springer Japan 2016

Authors and Affiliations

  • Y. Zhu
    • 1
  • J. Ishizaka
    • 2
  • S. C. Tripathy
    • 3
  • S. Wang
    • 4
  • Y. Mino
    • 2
  • T. Matsuno
    • 5
  • D. J. Suggett
    • 6
  1. 1.Graduate School of Environmental StudiesNagoya UniversityNagoyaJapan
  2. 2.Institute for Space-Earth Environmental ResearchNagoya UniversityNagoyaJapan
  3. 3.National Centre for Antarctic and Ocean Research, Earth System Science OrganizationMinistry of Earth SciencesVasco-Da-GamaIndia
  4. 4.School of Marine SciencesNanjing University of Information Science and TechnologyNanjingChina
  5. 5.Research Institute for Applied MechanicsKyushu UniversityFukuokaJapan
  6. 6.Plant Functional Biology and Climate Change ClusterUniversity of Technology SydneyBroadwayAustralia

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