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Photosynthetic physiologies of phytoplankton in the eastern equatorial Indian Ocean during the spring inter-monsoon

  • Chao Yuan
  • Zongjun Xu
  • Xuelei ZhangEmail author
  • Qinsheng Wei
  • Huiwu Wang
  • Zongling Wang
Article

Abstract

Phytoplankton physiologies are dynamic and have sensitive responses to the ambient environment. In this paper, we examine photosynthetic physiologies of phytoplankton communities with Phyto-PAM in the eastern equatorial Indian Ocean during the spring inter-monsoon. Environmental parameters were measured to investigate the coupling between phytoplankton photosynthetic physiologies and their habitats. During the cruise, the water column was highly stratified. The mixed layer extended to about 75 m and was characterized by high temperature (>28°C) and low nutrient level. The Fv/Fm values and chlorophyll a (Chl a) concentrations were lower at the surface, as consequences of nutrient depletion and photo-inhibition. Subsurface Chl a maximum (SCM) occurred between 75 and 100 m, and had the highest Fv/Fm values. The formation of SCM was a balance between nutrient availability and light limitation. The SCM may contribute significantly to pelagic food web and primary production in the water column. Phytoplankton in different layers encountered different light, trophic and hydrographic dynamics and evolved distinct photosynthetic characteristics. Despite of co-limitation of nutrient limitation and photo-inhibition, phytoplankton in the surface layer showed their acclimation to high irradiance, had lower light utilization efficiencies (α: 0.061±0.032) and could exploit a wide range of light irradiance. Whereas, phytoplankton in the SCM layers presented the highest light utilization efficiencies (α: 0.146±0.48), which guaranteed higher photosynthetic capacities under low light level. These results provide insights into phytoplankton photo-adaption strategies in this less explored region.

Key words

Fv/Fm rapid light curves photosynthetic physiologies eastern equatorial Indian Ocean 

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Notes

Acknowledgements

We are grateful to the captain and crew of the R/V Madidihang 03 for their assistance during the cruise. We thank Kaiming Sun for his assistance on the draft, Jingyu Zhang for her guidance on obtaining remote sensing data.

References

  1. Barlow R, Lamont T, Gibberd M J, et al. 2017. Phytoplankton communities and acclimation in a cyclonic eddy in the southwest Indian Ocean. Deep Sea Research Part I: Oceanographic Research Papers, 124: 18–30, doi: 10.1016/j.dsr.2017.03.013CrossRefGoogle Scholar
  2. Bibby T S, Mary I, Nield J, et al. 2003. Low-light-adapted Prochlorococcus species possess specific antennae for each photosystem. Nature, 424(6952): 1051–1054, doi: 10.1038/nature01933CrossRefGoogle Scholar
  3. Bouchard J N, Campbell D A, Roy S. 2005. Effects of UV-B radiation on the D1 protein repair cycle of natural phytoplankton communities from three latitudes (Canada, Brazil, and Argentina). Journal of Phycology, 41(2): 273–286, doi: 10.1111/(ISSN)1529-8817CrossRefGoogle Scholar
  4. Cullen J J. 2015. Subsurface chlorophyll maximum layers: Enduring enigma or mystery solved?. Annual Review of Marine Science, 7(1): 207–239, doi: 10.1146/annurev-marine-010213-135111CrossRefGoogle Scholar
  5. Durako M J. 2012. Using PAM fluorometry for landscape-level assessment of Thalassia testudinum: Can diurnal variation in photochemical efficiency be used as an ecoindicator of seagrass health?. Ecological Indicators, 18: 243–251, doi: 10.1016/j.ecolind.2011.11.025CrossRefGoogle Scholar
  6. Edwards K F, Thomas M K, Klausmeier C A, et al. 2015. Light and growth in marine phytoplankton: allometric, taxonomic, and environmental variation. Limnology and Oceanography, 60(2): 540–552, doi: 10.1002/lno.10033CrossRefGoogle Scholar
  7. Eilers P H C, Peeters J H C. 1988. A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecological Modelling, 42: 199–215, doi: 10.1016/0304-3800(88)90057-9CrossRefGoogle Scholar
  8. Fernand L, Weston K, Morris T, et al. 2013. The contribution of the deep chlorophyll maximum to primary production in a seasonally stratified shelf sea, the North Sea. Biogeochemistry, 113(1-3): 153–166, doi: 10.1007/s10533-013-9831-7Google Scholar
  9. Field C B, Behrenfeld M J, Randerson J T, et al. 1998. Primary production of the biosphere: Integrating terrestrial and oceanic components. Science, 281(5374): 237–240, doi: 10.1126/science.281.CrossRefGoogle Scholar
  10. George J V, Nuncio M, Chacko R, et al. 2013. Role of physical processes in chlorophyll distribution in the western tropical Indian Ocean. Journal of Marine Systems, 113–114: 1–12, doi: 10.1016/j.jmarsys.2012.12.001Google Scholar
  11. Halsey K H, Jones B M. 2015. Phytoplankton strategies for photosynthetic energy allocation. Annual Review of Marine Science, 7(1): 265–297, doi: 10.1146/annurev-marine-010814-015813CrossRefGoogle Scholar
  12. Halsey K H, Milligan A J, Behrenfeld M J. 2014. Contrasting strategies of photosynthetic energy utilization drive lifestyle strategies in ecologically important picoeukaryotes. Metabolites, 4(2): 260–280, doi: 10.3390/metabo4020260CrossRefGoogle Scholar
  13. Hanson C E, Pattiaratchi C B, Waite A M. 2005. Sporadic upwelling on a downwelling coast: Phytoplankton responses to spatially variable nutrient dynamics off the Gascooyne region of Western Australia. Continental Shelf Research, 25: 1561–1582, doi: 10.1016/j.csr.2005.04.003CrossRefGoogle Scholar
  14. Harrison J W, Silsbe G M, Smith R E H. 2015. Photophysiology and its response to visible and ultraviolet radiation in freshwater phytoplankton from contrasting light regimes. Journal of Plankton Research, 37(2): 472–488, doi: 10.1093/plankt/fbv003CrossRefGoogle Scholar
  15. Hartig P, Wolfstein K, Lippemeier S, et al. 1998. Photosynthetic activity of natural microphytobenthos populations measured by fluorescence (PAM) and 14C-tracer methods: a comparison. Marine Ecology Progress Series, 166: 53–62, doi: 10.3354/mepsCrossRefGoogle Scholar
  16. Hong Lisha, Wang Chunsheng, Zhou Yadong, et al. 2012. The distribution of chlorophyll a in the tropical eastern Indian Ocean in austral summer. Acta Oceanologica Sinica, 31(5): 146–159, doi: 10.1007/s13131-012-0244-6CrossRefGoogle Scholar
  17. Hopkinson B M, Mitchell B G, Reynolds R A, et al. 2007. Iron limitation across chlorophyll gradients in the southern Drake Passage: Phytoplankton responses to iron addition and photosynthetic indicators of iron stress. Limnology and Oceanography, 52(6): 2540–2554, doi: 10.4319/lo.2007.52.6.2540CrossRefGoogle Scholar
  18. Idso S B, Gilbert R G. 1974. On the universality of the poole and atkins secchi disk-light extinction equation. Journal of Applied Ecology, 11(1): 399–401, doi: 10.2307/2402029CrossRefGoogle Scholar
  19. Ihnken S, Eggert A, Beardall J. 2010. Exposure times in rapid light curves affect photosynthetic parameters in algae. Aquatic Botany, 93(3): 185–194, doi: 10.1016/j.aquabot.2010.07.002CrossRefGoogle Scholar
  20. Kalaji H M, Carpentier R, Allakhverdiev S I, et al. 2012. Fluorescence parameters as early indicators of light stress in barley. Journal of Photochemistry and Photobiology B: Biology, 112: 1–6, doi: 10.1016/j.jphotobiol.2012.03.009CrossRefGoogle Scholar
  21. Kim Tiam S, Laviale M, Feurtet-Mazel A, et al. 2015. Herbicide toxicity on river biofilms assessed by pulse amplitude modulated (PAM) fluorometry. Aquatic Toxicology, 165: 160–171, doi: 10.1016/j.aquatox.2015.05.001CrossRefGoogle Scholar
  22. Lavaud J. 2007. Fast regulation of photosynthesis in diatoms: Mechanisms, evolution and ecophysiology. Functional Plant Science and Biotechonology, 1: 267–287Google Scholar
  23. Lavaud J, Strzepek R F, Kroth P G. 2007. Photoprotection capacity differs among diatoms: Possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate. Limnology and Oceanography, 52(3): 1188–1194, doi: 10.4319/lo.2007.52.3.1188CrossRefGoogle Scholar
  24. Lee K, Matsuno T, Endoh T, et al. 2017. A role of vertical mixing on nutrient supply into the subsurface chlorophyll maximum in the shelf region of the East China Sea. Continental Shelf Research, 143: 139–150, doi: 10.1016/j.csr.2016.11.001CrossRefGoogle Scholar
  25. Li Gang, Lin Qiang, Ni Guangyan, et al. 2012. Vertical patterns of early summer chlorophyll a concentration in the Indian Ocean with special reference to the variation of deep chlorophyll maximum. Journal of Marine Biology, 2012: Article ID 801248CrossRefGoogle Scholar
  26. Li Junlei, Sun Xiaoxia. 2014. Photosynthetic characteristics of phytoplankton in winter in the Jiaozhou Bay. Oceanologia et Limnologia Sinica (in Chinese), 45: 468–479Google Scholar
  27. Li Junlei, Sun Xiaoxia, Zheng Shan. 2016. In situ study on photosynthetic characteristics of phytoplankton in the Yellow Sea and East China Sea in summer 2013. Journal of Marine Systems, 160: 94–106, doi: 10.1016/j.jmarsys.2016.03.016CrossRefGoogle Scholar
  28. Lippemeier S, Hintze R, Vanselow K, et al. 2001. In-line recording of PAM fluorescence of phytoplankton cultures as a new tool for studying effects of fluctuating nutrient supply on photosynthesis. European Journal of Phycology, 36(1): 89–100, doi: 10.1080/09670260110001735238CrossRefGoogle Scholar
  29. Liu Huaxue, Ke Zhixin, Song Xingyu, et al. 2011. Primary production in the Bay of Bengal during spring intermonsoon period. Acta Ecologica Sinica (in Chinese), 31(23): 7007–7012Google Scholar
  30. Madhupratap M, Gauns M, Ramaiah N, et al. 2003. Biogeochemistry of the Bay of Bengal: physical, chemical and primary productivity characteristics of the central and western Bay of Bengal during summer monsoon 2001. Deep Sea Research Part II: Topical Studies in Oceanography, 50(5): 881–896, doi: 10.1016/S0967-0645(02)00611-2CrossRefGoogle Scholar
  31. Martin J, Tremblay J, Gagnon J, et al. 2010. Prevalence, structure and properties of subsurface chlorophyll maxima in Canadian Arctic waters. Marine Ecology Progress Series, 412: 69–84, doi: 10.3354/meps08666CrossRefGoogle Scholar
  32. McMinn A, Hegseth E N. 2004. Quantum yield and photosynthetic parameters of marine microalgae from the southern Arctic Ocean, Svalbard. Journal of the Marine Biological Association of the UK, 84(5): 865–871, doi: 10.1017/S0025315404010112hCrossRefGoogle Scholar
  33. Mino Y, Matsumura S, Lirdwitayaprasit T, et al. 2014. Variations in phytoplankton photo-physiology and productivity in a dynamic eutrophic ecosystem: a fast repetition rate fluorometer-based study. Journal of Plankton Research, 36(2): 398–411, doi: 10.1093/plankt/fbt118CrossRefGoogle Scholar
  34. Moore C M, Seeyave S, Hickman A E, et al. 2007. Iron-light interactions during the CROZet natural iron bloom and EXport experiment (CROZEX) I: Phytoplankton growth and photophysiology. Deep Sea Research Part II: Topical Studies in Oceanography, 54(18–20): 2045–2065, doi: 10.1016/j.dsr2.2007.06.011CrossRefGoogle Scholar
  35. Moore C M, Suggett D J, Hickman A E, et al. 2006. Phytoplankton photoacclimation and photoadaptation in response to environmental gradients in a shelf sea. Limnology and Oceanography, 51(2): 936–949, doi: 10.4319/lo.2006.51.2.0936CrossRefGoogle Scholar
  36. Parsons T R, Maita Y, Lalli C M. 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Toronto, Canada: Pergamon PressGoogle Scholar
  37. Ralph P J, Gademann R. 2005. Rapid light curves: a powerful tool to assess photosynthetic activity. Aquatic Botany, 82(3): 222–237, doi: 10.1016/j.aquabot.2005.02.006CrossRefGoogle Scholar
  38. Rao R R, Kumar M S G, Ravichandran M, et al. 2010. Interannual variability of Kelvin wave propagation in the wave guides of the equatorial Indian Ocean, the coastal Bay of Bengal and the southeastern Arabian Sea during 1993–2006. Deep Sea Research Part I: Oceanographic Research Papers, 57(1): 1–13, doi: 10.1016/j.dsr.2009.10.008CrossRefGoogle Scholar
  39. Ryan K G, Cowie R O M, Liggins E, et al. 2009. The short-term effect of irradiance on the photosynthetic properties of Antarctic fast-ice microalgal communities. Journal of Phycology, 45(6): 1290–1298, doi: 10.1111/j.1529-8817.2009.00764.xCrossRefGoogle Scholar
  40. Sardessai S, Shetye S, Maya M V, et al. 2010. Nutrient characteristics of the water masses and their seasonal variability in the eastern equatorial Indian Ocean. Marine Environmental Research, 70(3–4): 272–282, doi: 10.1016/j.marenvres.2010.05.009CrossRefGoogle Scholar
  41. Schott F A, McCreary J P Jr. 2001. The monsoon circulation of the In-dian Ocean. Progress in Oceanography, 51(1): 1–123, doi: 10.1016/S0079-6611(01)00083-0CrossRefGoogle Scholar
  42. Schreiber U. 2004. Pulse-Amplitude-Modulation (PAM) fluorometry and saturation pulse method: An overview. In: Papageorgiou G C, Govindjee, eds. Chlorophyll a Fluorescence. Advances in Photosynthesis and Respiration, vol 19. Netherlands: Springer, 279–319Google Scholar
  43. Schreiber U, Bilger W, Neubauer C. 1995. Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze E D, Caldwell M M, eds. Ecophysiology of Photosynthesis. Berlin, Heidelberg: Springer, 49–70Google Scholar
  44. Sharon Y, Beer S. 2008. Diurnal movements of chloroplasts in Halophila stipulacea and their effect on PAM fluorometric measurements of photosynthetic rates. Aquatic Botany, 88(4): 273–276, doi: 10.1016/j.aquabot.2007.11.006CrossRefGoogle Scholar
  45. Sharples J, Moore M C, Rippeth T P, et al. 2001. Phytoplankton distribution and survival in the thermocline. Limnology and Oceanography, 46(3): 486–496, doi: 10.4319/lo.2001.46.3.0486CrossRefGoogle Scholar
  46. Six C, Finkel Z V, Rodriguez F, et al. 2008. Contrasting photoacclimation costs in ecotypes of the marine eukaryotic picoplankter Ostreococcus. Limnology and Oceanography, 53(1): 255–265, doi: 10.4319/lo.2008.53.1.0255CrossRefGoogle Scholar
  47. Strutton P G, Coles V J, Hood R R, et al. 2014. Biogeochemical variability in the equatorial Indian Ocean during the monsoon transition. Biogeosciences Discussions, 11: 6185–6219, doi: 10.5194/bgd-11-6185-2014CrossRefGoogle Scholar
  48. Suggett D J, Prášil O, Borowitzka M A. 2010. Chlorophyll a Fluorescence in Aquatic Sciences: Methods and Applications. Dordrecht, Netherlands: SpringerCrossRefGoogle Scholar
  49. Thompson P A, Pesant S, Waite A M. 2007. Contrasting the vertical differences in the phytoplankton biology of a dipole pair of eddies in the south-eastern Indian Ocean.Deep Sea Research Part II: Topical Studies in Oceanography, 54(8-10): 1003–1028, doi: 10.1016/j.dsr2.2006.12.009Google Scholar
  50. Wagner H, Jakob T, Wilhelm C. 2006. Balancing the energy flow from captured light to biomass under fluctuating light conditions. New Phytologist, 169(1): 95–108, doi: 10.1111/nph.2006.169.issue-1CrossRefGoogle Scholar
  51. Wang Xiaodong, Jiang Tao, Cen Jingyi, et al. 2012. Photosynthetic characteristics of phytoplankton in the Daya Bay. Oceanologia et Limnologia Sinica (in Chinese), 43: 589–594Google Scholar
  52. White S, Anandraj A, Bux F. 2011. PAM fluorometry as a tool to assess microalgal nutrient stress and monitor cellular neutral lipids. Bioresource Technology, 102(2): 1675–1682, doi: 10.1016/j.biortech.2010.09.097CrossRefGoogle Scholar
  53. Wiggert J D, Murtugudde R G, Christian J R. 2006. Annual ecosystem variability in the tropical Indian Ocean: Results of a coupled bio-physical ocean general circulation model. Deep Sea Research Part II: Topical Studies in Oceanography, 53(5–7): 644–676, doi: 10.1016/j.dsr2.2006.01.027CrossRefGoogle Scholar
  54. Wyrtki K. 1973. An equatorial jet in the Indian Ocean. Science, 181(4096): 262–264, doi: 10.1126/science.181.4096.262CrossRefGoogle Scholar
  55. Xue Bing, Sun Jun, Ding Changling, et al. 2016. Diatom communities in equatorial region and its adjacent areas of eastern Indian Ocean during spring intermonsoon 2014. Haiyang Xuebao (in Chinese), 38(2): 112–120Google Scholar
  56. Zhang Min, Kong Fanxiang, Wu Xiaodong, et al. 2008. Different photochemical responses of phytoplankters from the large shallow Taihu Lake of subtropical China in relation to light and mixing. Hydrobiologia, 603(1): 267–278, doi: 10.1007/s10750-008-9277-4CrossRefGoogle Scholar
  57. Zhang Wenquan, Wang Baodong, Wei Qinsheng, et al. 2016. Spatial distribution of primary nitrite maximum and its influencing factors in the east Indian Ocean in spring. Advances in Marine Science (in Chinese), 34(3): 403–410Google Scholar
  58. Zhou Yadong, Wang Chunsheng, Wang Xiaogu, et al. 2011. The distribution of size-fractionated chlorophyll a in the Indian Ocean South Equatorial Current. Acta Ecologica Sinica (in Chinese), 31(16): 4586–4598Google Scholar

Copyright information

© Chinese Society for Oceanography and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Chao Yuan
    • 1
    • 2
  • Zongjun Xu
    • 2
  • Xuelei Zhang
    • 2
    Email author
  • Qinsheng Wei
    • 2
  • Huiwu Wang
    • 3
  • Zongling Wang
    • 1
    • 2
  1. 1.College of Environment Science and EngineeringOcean University of ChinaQingdaoChina
  2. 2.Marine Ecology Research Center, MNR Key Laboratory of Science and Engineering for Marine Ecosystems, First Institute of OceanographyMinistry of Natural ResourcesQingdaoChina
  3. 3.MNR Key Laboratory of Marine Science and Numerical Modeling, First Institute of OceanographyMinistry of Natural ResourcesQingdaoChina

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