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The Phenomenon Of Emiliania Huxleyi In Aspects Of Global Climate And The Ecology Of The World Ocean

https://doi.org/10.24057/2071-9388-2020-214

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Abstract

Emiliania huxleyi (Lohmann) evolved from the genus Gephyrocapsa Kamptner (Prymneosiophyceae) of the coccolithophore family Naёlaerhadaceae. Over the past 100 thousand years E. huxleyi has acquired the status of the most ecologically predominant coccolithophore due to its remarkable adaptability to a variety of environmental conditions and interspecific competitiveness. E. huxleyi plays an important role in both the marine carbon system and carbon cycling between the atmosphere and ocean due to its ability to produce organic and inorganic carbon as well as to form massive blooms throughout the world ocean. This study examines both older information and recent findings to shed light on the current tendencies in the two-way interactions between E. huxleyi blooms and the immediate and global environment under conditions of climate change. The assembled knowledge has emerged from laboratory and mesocosm instrumental investigations, retrievals of satellite remote sensing data, machine learning/statistical analyses, and numerical simulations. Special attention is given to both the quantitative data reported over the last two decades on such interactions, and the only very recently appearing mid-term projections of E. huxleyi bloom dynamics across the world ocean. These blooms strongly affect the atmosphere and ocean carbon cycles. They reduce CO2 fluxes from by ~50% to ~150% as is documented for the North Atlantic, and on the global scale release particulate inorganic carbon as calcium calcite in the amounts assessed at 0.4 to 4.8 PgC/yr. At the same time, they are also sensitive to the atmospheric and oceanic state. This results in E. huxleyi blooms having an increased impact on the environment in response to ongoing global warming.

About the Authors

Dmitry V. Pozdnyakov
Nansen International Environmental and Remote Sensing Centre; St. Petersburg State University
Russian Federation

14th Line 7, Vasilievsky Island, St. Petersburg, 199034; 7/9 Universitetskaya nab., St. Petersburg, 199034



Natalia V. Gnatiuk
Nansen International Environmental and Remote Sensing Centre
Russian Federation

14th Line 7, Vasilievsky Island, St. Petersburg, 199034



Richard Davy
Nansen Environmental and Remote Sensing Center
Norway

Thormøhlens gate 47, Bergen, N-5006



Leonid P. Bobylev
Nansen International Environmental and Remote Sensing Centre
Russian Federation

Nansen International Environmental and Remote Sensing Centre

14th Line 7, Vasilievsky Island, St. Petersburg, 199034



References

1. Alcolombri U., Ben-Dor S., Feldmesser E., Levi Y, Tawfik D. S. and Vardi A. (2015). Identification of the algal dimethyl sulfide-releasing enzyme: A missing link in the marine sulfur cycle. Science, 348(6242), 1466-1469, DOI: 10.1126/science.aab1586.

2. Alekin O. (1966). Ocean chemistry. Leningrad: Gidrometizdat, 344p. (in Russian).

3. Alexander H., Rouco M., Sheean T. H. and Dyhrman S. T. (2020). Transcriptional response of Emiliania huxleyi under changing nutrient environments in the North Pacific Subtropical Gyre. Environmental Microbiology, 22(5), 1847-1860, DOI: 10.1111/1462-2920.14942.

4. Althoff F., Benzing K., Comba P, McRoberts C., Boyd D. R., Greiner S. and Keppler F. (2014). Abiotic methanogenesis from organosulphur compounds under ambient conditions. Nature Communications, 5(1), 1-9, DOI: 10.1038/ncomms5205.

5. Amelina A., Segeeva V., Arashkevich E., Drifts A., Louppova N. and Solovyev K. (2017). Feeding of the dominant herbivorous plankton species in the Black Sea and their role in coccolithophorid consumption. Oceanology, 57(6), 806-816, DOI: 10.1134/S000143701706011X.

6. Bach L.T., Riebesell U. and Schulz K. G. (2011). Distinguishing between the effects of ocean acidification and ocean carbonation in the coccolithophore Emiliania huxleyi. Limnology and Oceanography, 56(6), 2040-2050, DOI: 10.4319/lo.2011.56.6.2040.

7. Bach L.T., Mackinder L.C., Schulz K.G., Wheeler G., Schroeder D.C., Brownlee C. and Riebesell U. (2013). Dissecting the impact of CO2 and pH on the mechanisms of photosynthesis and calcification in the coccolithophore Emiliania huxleyi. New Phytologist, 199(1), 121-134, DOI: 10.1111/nph.12225.

8. Bach L.T., Riebesell U., Gutowska M.A., Federwisch L. and Schulz K.G. (2015). A unifying concept of coccolithophore sensitivity to changing carbonate chemistry embedded in an ecological framework. Progress in Oceanography, 135, 125-138, DOI: 10.1016/j.pocean.2015.04.012.

9. Balch W.M., Bowler B.C., Lubelczyk L.C. and Stevens M.W. (2014). Aerial extent, composition, bio-optics and biogeochemistry of a massive under-ice algal bloom in the Arctic. Deep-Sea Research II, 105, 42-58, DOI: 10.1016/j.dsr2.2014.04.001.

10. Balch W.M., Kilpatrick K., Holligan P.M. and Cucci T. (1993). Coccolith production and detachment by Emiliania huxleyi (Prymnesiophyceae). Journal of Phycology, 29(5), 566-575, DOI: 10.1111/j.0022-3646.1993.00566.x.

11. Balch W.M., Bates N.R., Lam PJ., Twining B.S., Rosengard S.Z., Bowler B.C., Drapeau D.T., Garley R., Lubelczyk L.C., Mitchell C. and Rauschenberg S. (2016). Factors regulating the Great Calcite Belt in the Southern Ocean and its biogeochemical significance. Global Biogeochemical Cycles, 30(8), 1124-1144, DOI: 10.1002/2016GB005414.

12. Benner I., Diner R.E., Lefebvre S.C., Li D., Komada T., Carpenter E.J. and Stillman J.H. (2013). Emiliania huxleyi increases calcification but not expression of calcification-related genes in long-term exposure to elevated temperature and pCO2. Philosophical Transactions of the Royal Society B, 368(1627), 20130049, DOI: 10.1098/rstb.2013.0049.

13. Boyd P.W. and Hutchins D.A. (2012). Understanding the responses of ocean biota to a complex matrix of cumulative anthropogenic change. Marine Ecology Progress Series, 470, 125-135, DOI: 10.3354/meps10121.

14. Brown C. and Yoder J. (1994). Coccolithophorid blooms in the Global ocean. Journal of Geophysical Research, 99(C4): 7467-7482, DOI: 10.1029/93JC02156.

15. Brownlee C. and Taylor A. (2004). Calcification in coccolithophores: A cellular perspective. In: H. R. Thierstein, J. R. Young, ed., Coccolithophores. Springer, Berlin, Heidelberg, 31-49, DOI: 10.1007/978-3-662-06278-4_2.

16. Brownlee C., Wheeler G.L. and Taylor A.R. (2015). Coccolithophore biomineralization: New questions, new answers. Seminars in Cell & Developmental Biology, 46, 11-16, DOI: 10.1016/j.semcdb.2015.10.027.

17. Burenkov V.I., Kopelevich O.V., Rat'kova T.N. and Sheberstov S.V. (2011). Satellite observations of coccolithophorids in the Barents Sea. Okeanologiya. 51(5), 818-826 (in Russian).

18. Charalampopoulou A., Poulton A.J., Bakker D.C., Lucas M.I., Stinchcombe M.C. and Tyrrell T. (2016). Environmental drivers of coccolithophore abundance and calcification across Drake Passage (Southern Ocean). Biogeosciences, 13(21), 5917-5935, DOI: 10.5194/bg-13-5917-2016.

19. Cokacar T., Oguz T. and Kubilay N. (2004). Satellite-detected early summer coccolithophore blooms and their interannual variability in the Black Sea. Deep-Sea Research I, 51(8), 1017-1031, DOI: 10.1016/j.dsr.2004.03.007.

20. Daniels C.J., Poulton A.J., Balch W.M., Maranon E., Adey T., Bowler B.C. and Tyrrell T. (2018). A global compilation of coccolithophore calcification rates. Earth System Science Data, 10(4), 1859-1876, DOI: 10.5194/essd-10-1859-2018.

21. Dlugokencky E. (2016). Annual Mean Carbon Dioxide Data. Earth System Research Laboratory, National Oceanic & Atmospheric Administration.

22. Durairaj P, Sarangi R.K., Ramalingam S., Thirunavukarassu T. and Chauhan P. (2015). Seasonal nitrate algorithms for nitrate retrieval using OCEANSAT-2 and MODIS-AQUA satellite data. Environmental Monitoring and Assessment, 187(4), 1-15, DOI: 10.1007/s10661-015-4340-x.

23. Evans C., Kadner S., Darroch L., Wilson W., Liss P. and Malin G. (2007). The relative significance of viral lysis and microzooplankton grazing as pathways of dimethylsulphoniopropionate (DMSP) cleavage: An Emiliania huxleyi culture study, Limnological and Oceanographic Methods, 53(3), 1036-1045, DOI: 10.4319/lo.2007.52.3.1036.

24. Feng Y., Hare C. E., Leblanc K., Rose J. M., Zhang Y., DiTullio G. R. and Hutchins D. A. (2009). The effects of increased pCO2 and temperature on the North Atlantic spring bloom: I. Phytoplankton community and biogeochemical response. Marine Ecology Progress Series, 388, 13-25, DOI: 10.3354/meps08133.

25. Feng Y., Roleda M. Y., Armstrong E., Law C. S., Boyd P. W. and Hurd C. L. (2018). Environmental controls on the elemental composition of a Southern Hemisphere strain of the coccolithophore Emiliania huxleyi. Biogeosciences, 15(2), 581-595, DOI: 10.5194/bg-15-581-2018.

26. Fiorini S., Middelburg J. J. and Gattuso J.-P. (2011). Testing the effects of elevated pCO2 on coccolithophores (Prymnesiophyceae): comparison between haploid and diploid life stages. Journal of Phycology, 47(6), 1281-1291, DOI: 10.1111/j.1529-8817.2011.01080.x.

27. Frada M. J., Bidle K. D., Probert I. and de Vargas C. (2012). In situ survey of life cycle phases of the coccolithophore Emiliania huxleyi (Haptophyta). Environmental Microbiology, 14(6), 1558-1569, DOI: 10.1111/j.1462-2920.2012.02745.x.

28. Gao K., Ruan Z., Villafane V. E., Gattuso J. P. and Helbling E. W. (2009). Ocean acidification exacerbates the effect of UV radiation on the calcifying phytoplankter Emiliania huxleyi. Limnology and Oceanography, 54(6), 1855-1862, DOI: 10.4319/lo.2009.54.6.1855.

29. Gnatiuk N., Radchenko I., Davy R., Morozov E. and Bobylev L. (2020). Simulation of factors affecting Emiliania huxleyi blooms in Arctic and sub-Arctic seas by CMIP5 climate models: model validation and selection. Biogeosciences, 17(4), 1199-1212, DOI: 10.5194/bg-17-1199-2020.

30. Godoi R. H. M., Aerts K., Harlay J., Kaegi R., Ro C. U., Chou L. and van Grieken R. (2008). Organic surface coating on coccolithophores Emiliania huxleyi: Its determination and implication in the marine carbon cycle. Microchemical Journal, 91(2), 266-271, DOI: 10.1016/j.microc.2008.12.009.

31. Godrijan J., Drapeau D. and Balch W. M. (2020). Mixotrophic uptake of organic compounds by coccolithophores. Limnology and Oceanog raphy, 65(6), 1410-1421, DOI:10.1002/lno.11396.

32. Green J.C., Course PA and Tarran G.A. (1996). The life-cycle of Emiliania huxleyi: A brief review and a study of relative ploidy levels analysed by flow cytometry. Journal of Marine Systems, 9(1-2), 33-44, DOI: 10.1016/0924-7963(96)00014-0.

33. Hagino K., Bendif E.M., Young J.R., Kogame K., Probert I., Takano Y., Horiguchi T., Vargas C. and Okada H. (2011) New evidence for morphological and genetic variation in the cosmopolitan coccolithophore Emiliania huxleyi (Prymnesiophyceae) from the COX1b-ATP4 genes. Journal of Phycology, 47(5), 1164-1176, DOI: 10.1111/j.1529-8817.2011.01053.x.

34. Harris R. P (2004). Zooplankton grazing on the coccolithophore Emiliania huxleyi and its role in inorganic carbon flux. Marine Biology, 119, 431-49, DOI: 10.1007/BF00347540.

35. Hayden L. (2013). Effects of ocean acidification and nutrient enrichment on growth of the planktonic coccolithophore Emiliania huxleyi. Available at: https://www.mbl.edu/ses [Accessed 7 February 2021].

36. Iglesias-Rodriguez M.D., Halloran PR., Rickaby R.E., Hall I.R., Colmenero-Hidalgo E., Gittins J.R. and Boessenkool K.P. (2008). Phytoplankton calcification in a high-CO2 world. Science, 320 (5874), 336-340, DOI: 10.1126/science.1154122.

37. Iglesias-Rodriguez M.D., Schofield O.M., Batley J., Medlin L.K. and Hayes PK. (2006). Intraspecific genetic diversity in the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae): the use of microsatellite analysis in marine phytoplankton population studies. Journal of Phycology, 42(3), 526-536, DOI: 10.1111/j.1529-8817.2006.00231.x.

38. Johnsen S.A.L. and Bollmann J. (2020). Coccolith mass and morphology of different Emiliania huxleyi morphotypes: A critical examination using Canary Islands material. PLoS ONE, 15(3), e0230569, DOI: 10.1371/journal.pone.0230569.

39. Kaffes A., Thoms S., Trimborn S., Rost B., Langer G., Richter K. U. and Giordano M. (2010). Carbon and nitrogen fluxes in the marine coccolithophore Emiliania huxleyi grown under different nitrate concentrations. Journal of Experimental Marine Biology and Ecology, 393(1-2), 1-8, DOI: 10.1016/j.jembe.2010.06.004.

40. Klintzsch T., Langer G., Nehrke G., Wieland A., Lenhart K. and Keppler F. (2019). Methane production by three widespread marine phytoplankton species: release rates, precursor compounds and potential relevance for the environment. Biogeosciences, 16(20), 4129-4144, DOI: 10.5194/bg-16-4129-2019.

41. Kondrik D.V., Kazakov E.E., Pozdnyakov D.V. and Johannessen O.M. (2019). Satellite evidence for enhancement of columnal mixing ratio of atmospheric CO2 over E. huxleyi blooms. Transactions of the Karelian Research Centre of the Russian Academy of Sciences, 9, 125-135.

42. Kondrik D.V., Pozdnyakov D.V. and Johannessen O.M. (2018). Satellite evidence that E. huxleyi phytoplankton blooms weaken marine carbon sinks. Geophysical Research Letters, 45(2), 846-854, DOI: 10.1002/2017GL076240.

43. Kondrik D.V., Pozdnyakov D.V. and Pettersson L.H. (2017). Particulate inorganic carbon production within E. huxleyi blooms in subpolar and polar seas: a satellite time series study (1998-2013). International Journal of Remote Sensing, 38(22), 6179-6205, DOI: 10.1080/01431161.2017.1350304.

44. Kopelevich O., Burenkov V., Sheberstov S., Vazyulya S., Kravchishina M., Pautova L. and Grigoriev A. (2013). Satellite monitoring of coccolithophore blooms in the Black Sea from ocean color data. Remote Sensing of Environment, 146, 113-123, DOI: 10.1016/j.rse.2013.09.009.

45. Krumhardt K.M., Lovenduski N.S., Iglesias-Rodriguez M.D. and Kleypas J.A. (2017). Coccolithophore growth and calcification in a changing ocean. Progress in Oceanography, 159, 276-295, DOI: 10.1016/j.pocean.2017.10.007.

46. Kubryakov A. A., Mikaelyan A. S. and Stanichny S. V. (2019). Summer and winter coccolithophore blooms in the Black Sea and their impact on production of dissolved organic matter from Bio-Argo data. Journal of Marine Systems, 199, 103220, DOI: 10.1016/j.jmarsys.2019.103220.

47. Lana A., Bell T. G., Simo R., Vallina S. M., Ballabrera-Poy J., Kettle A. J. and Liss P S. (2011). An updated climatology of surface dimethylsulfide concentrations and emission fluxes in the global ocean. Global Biogeochemical Cycles, 25(1), GB1004, DOI: 10.1029/2010GB003850.

48. Lenhart K., Klintzsch T., Langer G., Nehrke G., Bunge M., Schnell S. and Keppler F. (2016). Evidence for methane production by the marine algae Emiliania huxleyi. Biogeosciences, 13(10), 3163-3174, DOI: 10.5194/bg-13-3163-2016.

49. Leon P, Walsham P, Bresnan E., Hartman S. E., Hughes S., Mackenzie K. and Webster L. (2018). Seasonal variability of the carbonate system and coccolithophore Emiliania huxleyi at a Scottish Coastal Observatory monitoring site. Estuarine, Coastal and Shelf Science, 202, 302-314, DOI: 10.1016/j.ecss.2018.01.011.

50. Lipsen M.S., Crawford D.W., Gower J. and Harrison PJ. (2007). Spatial and temporal variability in coccolithophore abundance and production of PIC and POC in the NE subarctic during El Nino (1998) and La Nina (1999) and 2000. Progress in Oceanology, 75(2), 304-325, DOI: 10.1016/j.pocean.2007.08.004.

51. Loebl M., Cockshutt A.M., Campbell D.A. and Finkel Z.V. (2010). Physiological basis for high resistance to photoinhibition under nitrogen depletion in Emiliania huxleyi. Limnology and Oceanography, 55(5), 2150-2160, DOI: 10.4319/lo.2010.55.5.2150.

52. Lohbeck K.T., Riebesell U. and Reusch T.B.H. (2012). Adaptive evolution of a key phytoplankton species to ocean acidification. Nature Geosciences, 5, 346-351, DOI: 10.1038/ngeo1441.

53. Lorenzo M.R., Neale PJ., Sobrino C., Leon P, Vazquez V., Bresnan E. and Segovia M. (2019). Effects of elevated CO2 on growth, calcification, and spectral dependence of photoinhibition in the coccolithophore Emiliania huxleyi (Prymnesiophyceae). Journal of Phycology, 55(4), 775788, DOI: 10.1111/jpy.12885.

54. Mackinder L., Wheeler G., Schroeder D., von Dassow P., Riebesell U. and Brownlee C. (2011). Expression of biomineralization-related ion transport genes in Emiliania huxleyi. Environmental Microbiology, 13(12), 3250-3265, DOI: 10.1111/j.1462-2920.2011.02561.x.

55. Malin G. and Steinke M. (2004). Dimethyl sulfide production: what is the contribution of the coccolithophores? In: H. Thierstein and J. Young, ed., Coccolithophores, Heidelberg: Springer, Berlin, Heidelberg, 127-164, DOI: 10.1007/978-3-662-06278-4_6.

56. Maranon E., Balch W. M., Cermeno P, Gonzalez N., Sobrino C., Fernandez A. and Pelejero C. (2016). Coccolithophore calcification is independent of carbonate chemistry in the tropical ocean. Limnology and Oceanology, 61(4), 1345-1357, DOI: 10.1002/lno.10295.

57. Martin J.H., Coale K.H., Johnson K.S., Fitzwater S.E., Gordon R.M., Tanner S.J. and Tindale N. W. (1994). Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature, 371, 123-129, DOI: 10.1038/371123a0.

58. Martiny A.C., Vrugt J.A. and Lomas M.W. (2014). Concentrations and ratios of particulate organic carbon, nitrogen, and phosphorus in the global ocean. Scientific Data, 1, 140048, DOI: 10.1038/sdata.2014.48.

59. Merico A., Tyrrell T., Lessard E.J., Oguz T., Stabeno PJ., Zeeman S.I. and Whitledge T.E. (2004). Modelling phytoplankton succession on the Bering Sea shelf: role of climate influences and trophic interactions in generating Emiliania huxleyi blooms 1997-2000. Deep Sea Research Part I: Oceanographic Research Papers, 51, 1803-1826, DOI: 10.1016/j.dsr.2004.07.003.

60. Meyer J. and Riebesell U. (2015). Reviews and syntheses: Responses of coccolithophores to ocean acidification: a meta-analysis. Biogeosciences, 12(6), 1671-1682, DOI: 10.5194/bg-12-1671-2015.

61. Mikaelyan A.S., Pautova L.A., Chasovnikov V.K., Mosharov S.A. and Silkin V.A. (2015). Alternation of diatoms and coccolithophores in the north-eastern Black Sea: a response to nutrient changes. Hydrobiologia, 755(1), 89-105, DOI: 10.1007/s10750-015-2219-z.

62. Miller C.B., Frost B.W., Wheeler P.A., Landry M.R., Welschmeyer N. and Powell T.M. (1991). Ecological dynamics in subarctic Pacific, a possibly iron-limited ecosystem. Limnology and Oceanology, 36(8), 1600-1615, DOI: 10.4319/lo.1991.36.8.1600.

63. Mohan R., Mergulhao L.P., Guptha M.V.S., Rajakumar A., Thamban M., AnilKumar N. and Ravindra R. (2008). Ecology of coccolithophores in the Indian sector of the Southern Ocean. Marine Micropaleontology, 67(1-2), 30-45, DOI: 10.1016/j.marmicro.2007.08.005.

64. Moncheva S. and Krastev A. (1997). Some aspects of phytoplankton long-term alterations off Bulgarian Black Sea Shelf. In: E. Ozsoy, A. Mikaelyan, ed., Sensitivity to Change: Black Sea, Baltic Sea and North Sea. Dordrecht: Springer, Dordrecht, 79-93, DOI: 10.1007/978-94-011-5758-2_7.

65. Moore T.S., Dowel M.D. and Franz B.A. (2012). Detection of coccolithophore blooms in ocean color imagery: A generalized approach for use with multiple sensors. Remote Sensing of Environment, 117, 249-263, DOI: 10.1016/j.rse.2011.10.001.

66. Morozov E.A., Kondrik D.V., Chepikova S.S. and Pozdnyakov D.V. (2019). Atmospheric columnar CO2 enhancement over E. huxleyi blooms: case studies in the North Atlantic and Arctic waters. Limnology and Oceanology Series, 3, 28-33, DOI: 10.17076/lim989.

67. Morozov E., Pozdnyakov D.V., Smyth T., Sychev V. and Grassl H. (2013). Space-borne study of seasonal, multi-year and decadal phytoplankton dynamics in the Bay of Biscay. International Journal of Remote Sensing, 34(4), 1297-1331, DOI: 10.1080/01431161.2012.718462.

68. Muggli D.L. and Harrison PJ. (1996). Effects of nitrogen source on physiology and metal nutrition of Emiliania huxleyi grown under different iron and light conditions. Marine Ecology Progress Series, 130, 255-267, DOI: 10.3354/meps130255.

69. Müller M.N. (2019). On the Genesis and Function of Coccolithophore Calcification. Frontiers in Marine Science, 6, 49, DOI: 10.3389/fmars.2019.00049.

70. Müller M.N., Antia A.N. and LaRoche J. (2008). Influence of cell cycle phase on calcification in the coccolithophore Emiliania huxleyi. Limnology and Oceanography, 53(2), 506-512, DOI: 10.4319/lo.2008.53.2.0506.

71. Müller M.N., Trull T.W. and Hallegraeff G.M. (2015). Differing responses of three Southern Ocean Emiliania huxleyi ecotypes to changing seawater carbonate chemistry. Marine Ecology Progress Series, 531,81-90, DOI: 10.3354/meps11309.

72. Müller M.N., Beaufort L., Bernard O., Pedrotti M.L., Talec A. and Sciandra A. (2012). Influence of CO2 and nitrogen limitation on the coccolith volume of Emiliania huxleyi (Haptophyta). Biogeosciences, 9(10), 4155-4167, DOI: 10.5194/bg-9-4155-2012.

73. Nissen C., Vogt M., MQnnich M., Gruber N. and Haumann F.A. (2018). Factors controlling coccolithophore biogeography in the Southern Ocean. Biogeosciences, 15(22), 6997-7024, DOI: 10.5194/bg-15-6997-2018.

74. Oviedo A.M., Langer G. and Ziveri P. (2014). Effects of phosphorus limitation on coccoliths and elemental ratios in Mediterranean strains of the coccolithophore Emiliania huxleyi. Journal of Experimental Marine Biology and Ecology, 459, 105-113, DOI: 10.1016/j.jembe.2014.04.021.

75. Oziel L., Baudena A., Ardyna M., Massicotte P., Randelhoff A., Sallee J. B. and Babin M. (2020). Faster Atlantic currents drive poleward expansion of temperate phytoplankton in the Arctic Ocean. Nature Communications, 11(1), 1-8, DOI: 10.1038/s41467-020-15485-5.

76. Paasche E. (2002). A review of the coccolithophorid Emiliania huxleyi (Prymneosiophyceae) with particular reference to growth, coccolith formation, and calcification-photosynthesis interactions. Phycologia, 40(6), 503-529, DOI: 10.2216/i0031-8884-40-6-503.1.

77. Pantorno A., Holland D.P., Stojkovic S. and Beardall J. (2013). Impacts of nitrogen limitation on the sinking rate of the coccolithophorid Emiliania huxleyi (Prymneosiophyceae). Phycologia, 52(3), 288-294, DOI: 10.2216/12-064.1.

78. Petrenko D., Pozdnyakov D., Johannessen J., Counillon F. and Sychov V. (2013). Satellite-driven multi-year trend in primary production in the Arctic Ocean. International Journal of Remote Sensing, 34(11), 3903-3937, DOI: 10.1080/01431161.2012.762698.

79. Poulton A.J., Young J.R., Bates N.R. and Balch W. (2011). Biometry of detached Emiliania huxleyi coccoliths along the Patagonian Shelf. Marine Ecology Progress Series, 443, 1-17, DOI: 10.3354/meps09445.

80. Pozdnyakov D., Chepikova S. and Kondrik D. (2020). A possible teleconnection mechanism of initiation of Emiliania huxleyi outbursts in the Bering Sea in 1998-2001 and 2018-2019. Proceedings of SPIE, 11534, 1153412, DOI: 10.1117/12.2573272.

81. Pozdnyakov D., Kondrik D., Kazakov E. and Chepikova S. (2019). Environmental conditions favoring coccolithophore blooms in subarctic and arctic seas: a 20-year satellite and multi-dimensional statistical study. Proceedings of SPIE, 11150, 111501W, DOI: 10.1117/12.2547868.

82. Raffi I., Backman J., Fornaciari E., Palike H., Rio D., Lourens L. and Hilgen F. (2006). A review of calcareous nannofossil astrobiochronology encompassing the past 25 million years. Quaternary Science Reviews, 25(23-24), 3113-3137, DOI: 10.1016/j.quascirev.2006.07.007.

83. Ramos J.B., MQller M. and Riebesell U. (2010). Short-term response of the coccolithophore Emiliania huxleyi to an abrupt change in seawater carbon dioxide concentrations. Biogeosciences, 7(1), 177-186, DOI: 10.5194/bg-7-177-2010.

84. Read B.A., Kegel J., Klute M.J., Kuo A., Lefebvre S.C., Maumus F. and Grigoriev I.V. (2013). Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature, 499(7457), 209-213, DOI: 10.1038/nature12221.

85. Redfield A.C. (1934). On the proportions of organic derivatives in sea water and their relation to the composition of plankton. In: James Johnstone Memorial volume. Liverpool: University Press of Liverpool, 176-192.

86. Richier S., Fiorini S., Kerros M.E., von Dassow P. and Gattuso J.P (2010). Response of the calcifying coccolithophore Emiliania huxleyi to low pH/high pCO2: from physiology to molecular level. Marine Biology, 158(3), 551-560, DOI: 10.1007/s00227-010-1580-8.

87. Riebesell U., Zondervan I., Rost B., Tortell PD., Zeebe R.E. and Morel F.M. (2000). Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature, 407(6802), 364-367, DOI: 10.1038/35030078.

88. Riegman R., Stolte W., Noordeloos A.A.M. and Slezak D. (2000). Nutrient uptake and alkaline phosphatase (ec 3:1:3:1) activity of Emiliania huxleyi (Prymnesiophyceae) during growth under N and P limitation in continuous cultures. Journal of Phycology, 36(1), 87-96, DOI: 10.1046/j.1529-8817.2000.99023.x.

89. Rigual-Hernandez A.S., Trull T.W., Flores J.A., Nodder S.D., Eriksen R., Davies D.M., Hallegraeff G.M.F., Sierro J., Patil S.M., Cortina A., Ballegeer A.M., Northcote L.C., Abrantes F. and Rufino M.M. (2020). Full annual monitoring of Subantarctic Emiliania huxleyi populations reveals highly calcified morphotypes in high-CO2 winter conditions. Scientific Reports, 10, 2594-2599, DOI: 10.1038/s41598-020-59375-8.

90. Rivero-Calle S., Gnanadesikan A., Del Castillo C.E., Balch W.M. and Guikema S.D. (2015). Multidecadal increase in North Atlantic coccolithophores and potential role of rising CO2. Science, 350(6267), 1533-1537, DOI: 10.1126/science.aaa8026.

91. Rokitta S.D. and Rost B. (2012). Effects of CO2 and their modulation by light in the life-cycle stages of the coccolithophore Emiliania huxleyi. Limnology and Oceanography, 57(2), 607-618, DOI: 10.4319/lo.2012.57.2.0607.

92. Rost B. and Riebesell U. (2004). Coccolithophores and the biological pump: responses to environmental changes. In: H.R. Thierstein, J.R. Young, ed., Coccolithophores: from molecular processes to global impact. Heidelberg: Springer, Berlin, Heidelberg, 99-125, DOI: 10.1007/978-3-662-06278-4_5.

93. Sadeghi A., Dinter T., Vountas M., Taylor B., Altenburg-Soppa M. and Bracher A. (2012). Remote sensing of coccolithophore blooms in selected oceanic regions using the PhytoDOAS method applied to hyper-spectral satellite data. Biogeosciences, 9(6), 2127-2143, DOI: 10.5194/bg-9-2127-2012.

94. SchlQter L., Lohbeck K.T., Gutowska M.A., Groger J.P, Riebesell U. and ReuschT.B. (2014). Adaptation of a globally important coccolithophore to ocean warming and acidification. Nature Climate Change, 4(11), 1024-1030, DOI: 10.1038/nclimate2379.

95. Segovia M., Lorenzo M.R., Iniguez C. and Garcia-Gomez C. (2018). Physiological stress response associated with elevated CO2 and dissolved iron in a phytoplankton community dominated by the coccolithophore Emiliania huxleyi. Marine Ecology Progress Series, 586, 73-89, DOI: 10.3354/meps12389.

96. Sergeeva V.M., Drits A. and Flint M.V (2019). Specific features of distribution and nutrition of dominant zooplankton species under conditions of autumnal growth of coccolithophorids in the eastern Barents Sea. Oceanology, 59(5), 734-745 (in Russian), DOI: 10.31857/S0030-1574595734-745.

97. Sett S., Bach L.T., Schulz K.G., Koch-Klavsen S., Lebrato M. and Riebesell U. (2014). Temperature modulates coccolithophorid sensitivity of growth, photosynthesis and calcification to increasing seawater pCO2. PLoS ONE, 9(2), e88308, DOI: 10.1371/journal.pone.0088308.

98. Shi D., Xu Y. and Morel F. M. M. (2009). Effects of the pH/pCO2 control method on medium chemistry and phytoplankton growth. Biogeosciences, 6(7), 1199-1207, DOI: 10.5194/bg-6-1199-2009.

99. Shutler J.D., Land PE., Brown C.W., Findlay H. S., Donlon C.J., Medland M. and Blackford J. C. (2013). Coccolithophore surface distributions in the North Atlantic and their modulation of the air-sea flux of CO2 from 10 years of satellite Earth observation data. Biogeosciences, 10(4), 2699-2709, DOI: 10.5194/bg-10-2699-2013.

100. Silkin V.A. (2017). Why coccolithophorids dominate or the physiological mechanisms of Emiliania huxleyi domination. Voprosy sovremennoy al'gologii, [online] Volume 3(15). Available at: http://algology.ru/1185 [Accessed 03.11.2020] (in Russian with English summary).

101. Silkin V.A., Pautova L.A., Giordano M., Chasovnikov V.K., Vostokov S.V., Podymov O.I. and Moskalenko L.V. (2019). Drivers of phytoplankton blooms in the northeastern Black Sea. Marine Pollution Bulletin, 138, 274-284, DOI: /10.1016/j.marpolbul.2018.11.042.

102. Smith H.E., Poulton A.J., Garley R., Hopkins J., Lubelczyk L.C., Drapeau D.T. and Balch W. M. (2017). The influence of environmental variability on the biogeography of coccolithophores and diatoms in the Great Calcite Belt. Biogeosciences, 14(21), 4905-4925, DOI: 10.5194/bg-14-4905-2017.

103. Smyth T.J., Tyrrell T. and Tarrant B. (2004). Time series of coccolithophore activity in the Barents Sea, from twenty years of satellite imagery. Geophysical Research Letters, 31(11), L11302, DOI: 10.1029/2004GL019735.

104. Stelmakh L. and Gorbunova T. (2019). Emiliania huxleyi blooms in the Black Sea: Influence of abiotic and biotic factors. Botanica, 24(2), 172-184, DOI: 10.2478/botlit-2018-0017.

105. Strom S. L., Barberi O., Mazur C., Bright K. and Fredrickson K. (2020). High light stress reduces dinoflagellate predation on phytoplankton through both direct and indirect responses. Aquatic Microbial Ecology, 84, 43-57, DOI: 10.3354/ame01924.

106. Thierstein H.R. and Young J.R. (2004). Coccolithophores: from molecular processes to global Impact. Heidelberg: Springer-Verlag Berlin Heidelberg, 565 p., DOI: 10.1007/978-3-662-06278-4.

107. Thierstein H.R., Geitzenauer K.R., Molfino B. and Shackleton N.J. (1977). Global synchroneity of late Quaternary coccolith datum levels: validation by oxygen isotopes. Geology, 5(7), 400-404, DOI: 10.1130/0091-7613(1977)5<400:GSOLQC>2.0.CO;2.

108. Tyrrell T. and Merico A. (2004). Emiliania huxleyi: bloom observations and the conditions that induce them. In: H.R. Thierstein, J.R. Young, ed., Coccolithophores, 1st ed. Heidelberg: Springer-Verlag Berlin Heidelberg, 75-97, DOI: 10.1007/978-3-662-06278-4_4.

109. Tyrrell T. and Young J R. (2009). Coccolithophores. In: J. H. Steele, K. K. Turekian and S.A. Thorpe, ed., Encyclopedia of Ocean Sciences. 2nd ed. San Diego: Academic Press, 3568-3576, DOI: 10.2989/16085910109503736.

110. Vargas C., Aubry M.-P, Probert I. and Young J. (2007). Origin and Evolution of Coccolithophores: from Coastal Hunters to Oceanic Farmers. In: G. Falkowski, A. H. Knoll, ed., Evolution of Primary Producers in the Sea. Cambridge: Academic Press, 251-285, DOI: 10.1016/B978-012370518-1/50013-8.

111. Vogt M. and Liss PS. (2010). Dimethylsulfide and climate. Surface Ocean-Lower Atmospheric Processes. Geophysical Research Series, 187, 197-232, DOI: 10.1029/2008GM000790.

112. von Dassow P., Diaz-Rosas F., Bendif E.M., Gaitan-Espitia J. D., Mella-Flores D., Rokitta S. and Torres R. (2018). Over-calcified forms of the coccolithophore Emiliania huxleyi in high-CO2 waters are not preadapted to ocean acidification. Biogeosciences, 15(5), 1515-1534, DOI: 10.5194/bg-15-1515-2018.

113. von Dassow P., John U., Ogata H., Probert I., Bendif E.M., Kegel J.U. and De Vargas C. (2015). Life-cycle modification in open oceans accounts for genome variability in a cosmopolitan phytoplankton. The ISME Journal, 9(6), 1365-1377, DOI: 10.1038/ismej.2014.221.

114. Walker C.E., Taylor A.R., Langer G., Durak G.M., Heath S., Probert I. and Wheeler G.L. (2018). The requirement for calcification differs between ecologically important coccolithophore species. New Phytologist, 220(1), 147-162, DOI: 10.1111/nph.15272.

115. Wang S., Eliott S., Maltreed M. and Cameron-Smith P (2015) Influence of explicit Phaeocystis on the global distribution of marine dimethyl sulfide. Journal of Geophysical Research, 120(11), 2158-2177, DOI: 10.1002/2015JG003017.

116. Wang X., Fu F., Qu P, Kling J.D., Jiang H., Gao Y and Hutchins D. A. (2019). How will the key marine calcifier Emiliania huxleyi respond to a warmer and more thermally variable ocean? Biogeosciences, 16(22), 4393-4409, DOI: 10.5194/bg-16-4393-2019.

117. Winter A., Henderiks J., Beaufort L., Rickaby R.E. and Brown C.W. (2014). Poleward expansion of the coccolithophore Emiliania huxleyi. Journal of Plankton Research, 36(2), 316-325, DOI: 10.1093/plankt/fbt110.

118. Xu K. and Gao K. (2012). Reduced calcification decreases photoprotective capability in the coccolithophorid Emiliania huxleyi. Plant and Cell Physiology, 53(7), 1267-1274, DOI: 10.1093/pcp/pcs066.

119. Young J.R., Poulton A.J. and Tyrrell T. (2014). Morphology of Emiliania huxleyi coccoliths on the northwestern European shelf - is there an influence of carbonate chemistry? Biogeosciences, 11(17), 4771- 4782, DOI: 10.5194/bg-11-4771-2014.


For citation:


Pozdnyakov D.V., Gnatiuk N.V., Davy R., Bobylev L.P. The Phenomenon Of Emiliania Huxleyi In Aspects Of Global Climate And The Ecology Of The World Ocean. GEOGRAPHY, ENVIRONMENT, SUSTAINABILITY. 2021;14(2):50-62. https://doi.org/10.24057/2071-9388-2020-214

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