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Large-scale distribution of coccolithophores and Parmales in the surface waters of the Atlantic Ocean

Published online by Cambridge University Press:  20 December 2016

Qingshan Luan ,
Jianqiang Sun  and
Jun Wang
Qingshan Luan
Affiliation:
Division of Fishery Resources and Ecosystem, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China
Jianqiang Sun
Affiliation:
Division of Fishery Resources and Ecosystem, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China
Jun Wang*
Affiliation:
Division of Fishery Resources and Ecosystem, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China Function Laboratory for Marine Ecology and Environmental Sciences, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China
*
Correspondence should be addressed to: J. Wang, Division of Fishery Resources and Ecosystem, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China email: [email protected]
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Abstract

Coccolithophores and Parmales are important functional groups of calcified and siliceous marine nanophytoplankton. Large-scale biogeographic distributions of the two groups were investigated based on 71 samples that were collected in the Atlantic Ocean. Using a scanning electron microscope, a total of 48 taxa of coccolithophores and eight taxa of Parmales were recorded, with Emiliania huxleyi, Tetraparma pelagica and Triparma strigata as the predominant forms. The highest abundances of coccolithophores (376 × 103 cells l−1) and Parmales (624 × 103 cells l−1) were observed in waters north-east of the Falkland Islands and the South Georgia Island, in close association with the Subantarctic Front and Polar Front, respectively. Three major biogeographic assemblages, i.e. the Falkland Shelf Assemblage, the Southern Ocean Assemblage and the Atlantic Ocean Assemblage, were revealed in cluster analysis. Additionally, canonical correspondence analysis indicated that temperature significantly affects the latitudinal patterns of the two algal groups. High abundances of Parmales were closely coupled with those of E. huxleyi in waters of the Southern Ocean with low temperature (<10°C). However, the number of coccolithophore species, along with the Shannon–Weaver diversity, significantly increased with elevated temperature, suggesting more diverse assemblages in tropical waters.

Keywords

AbundanceAtlanticcoccolithophoresmultivariate analysisoceanic frontParmales
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 3 , May 2018 , pp. 567 - 579
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

REFERENCES

Ardyna, M., Babin, M., Gosselin, M., Devred, E., Rainville, L. and Tremblay, J.-É. (2014) Recent Arctic Ocean sea ice loss triggers novel fall phytoplankton blooms. Geophysical Research Letters 41, 6207–6212.CrossRefGoogle Scholar
Balch, W.M., Drapeau, D.T., Bowler, B.C., Lyczkowski, E.R., Lubelczyk, L.C., Painter, S.C. and Poulton, A.J. (2014) Surface biological, chemical, and optical properties of the Patagonian Shelf coccolithophore bloom, the brightest waters of the Great Calcite Belt. Limnology and Oceanography 59, 1715–1732.Google Scholar
Beaufort, L., Probert, I., de Garidel-Thoron, T., Bendif, E.M., Ruiz-Pino, D., Metzl, N., Goyet, C., Buchet, N., Coupel, P., Grelaud, M., Rost, B., Rickaby, R.E.M. and de Vargas, C. (2011) Sensitivity of coccolithophores to carbonate chemistry and ocean acidification. Nature 476, 80–83.Google Scholar
Boeckel, B. and Baumann, K.-H. (2008) Vertical and lateral variations in coccolithophore community structure across the subtropical frontal zone in the South Atlantic Ocean. Marine Micropaleontology 67, 255–273.Google Scholar
Bollmann, J., Cortés, M.Y., Haidar, A.T., Brabec, B., Close, A., Hofmann, R., Palma, S., Tupas, L. and Thierstein, H.R. (2002) Techniques for quantitative analyses of calcareous marine phytoplankton. Marine Micropaleontology 44, 163–185.Google Scholar
Booth, B.C., Lewin, J. and Norris, R.E. (1980) Siliceous nanoplankton. I. Newly discovered cysts from the Gulf of Alaska. Marine Biology 58, 205–209.Google Scholar
Booth, B.C. and Marchant, H.J. (1987) Parmales, a new order of marine chrysophytes, with descriptions of three new genera and seven new species. Journal of Phycology 23, 245–260.Google Scholar
Bown, P.R., Lees, J.A. and Young, J.R. (2004) Calcareous nannoplankton evolution and diversity through time. In Thierstein, H.R. and Young, J.R. (eds) Coccolithophores – from molecular processes to global impact. Berlin: Springer, pp. 481–508.Google Scholar
Boyce, D.G., Lewis, M.R. and Worm, B. (2010) Global phytoplankton decline over the past century. Nature 466, 591–596.Google Scholar
Brand, L.E. (1994) Physiological ecology of marine coccolithophores. In Winter, A. and Siesser, W.G. (eds) Coccolithophores. Cambridge: Cambridge University Press, pp. 39–49.Google Scholar
Bravo-Sierra, E. and Hernández-Becerril, D.U. (2003) Parmales (Chrysophyceae) from the Gulf of Tehuantepec, Mexico, including the description of a new species, Tetraparma insect sp. nov., and a proposal to the taxonomy of the group. Journal of Phycology 39, 577–583.Google Scholar
Buck, K.R. and Garrison, D.L. (1983) Protists from the ice-edge region of the Weddell Sea. Deep-Sea Research 30, 1261–1277.Google Scholar
Chen, B. (2015) Patterns of thermal limits of phytoplankton. Journal of Plankton Research 37, 285–292.Google Scholar
Dufrene, M. and Legendre, P. (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 67, 345–366.Google Scholar
Dutkiewicz, S., Morris, J.J., Follows, M.J., Scott, J., Levitan, O., Dyhrman, S.T. and Berman-Frank, I. (2015) Impact of ocean acidification on the structure of future phytoplankton communities. Nature Climate Change 5, 1002–1006. doi: 10.1038/nclimate2722.Google Scholar
Guillou, L., Chrétiennot-Dinet, M.J., Medlin, L.K., Claustre, H., Loiseaux-de-Goër, S. and Vaulot, D. (1999) Bolidomonas: a new genus with two species belonging to a new algal class, the Bolidophyceae (Heterokonta). Journal of Phycology 35, 368–381.Google Scholar
Hinz, D.J., Poulton, A.J., Nielsdόttir, M.C., Steigenberger, S., Korb, R.E., Achterberg, E.P. and Bibby, T.S. (2012) Comparative seasonal biogeography of mineralising nannoplankton in the Scotia Sea: Emiliania huxleyi, Fragilariopsis spp. and Tetraparma pelagica. Deep-Sea Research Part II 59–60, 57–66.Google Scholar
Honjo, S., Manganini, S.J., Krishfield, R.A. and Francois, R. (2008) Particulate organic carbon fluxes to the ocean interior and factors controlling the biological pump: a synthesis of global sediment trap programs since 1983. Progress in Oceanography 76, 217–285.Google Scholar
Ichinomiya, M., Dos Santos, A.L., Gourvil, P., Yoshikawa, S., Kamiya, M., Ohki, K., Audic, S., De Vargas, C., Noël, M.-H., Vaulot, D. and Kuwata, A. (2016) Diversity and oceanic distribution of the Parmales (Bolidophyceae), a picoplanktonic group closely related to diatoms. ISME Journal 10, 2419–2434. doi: 10.1038/ismej.2016.38.Google Scholar
Ichinomiya, M. and Kuwata, A. (2015) Seasonal variation in abundance and species composition of the Parmales community in the Oyashio region, western North Pacific. Aquatic Microbial Ecology 75, 207–223.CrossRefGoogle Scholar
Iglesias-Rodriguez, M.D., Halloran, P.R., Rickaby, R.E.M., Hall, I.R., Colmenero-Hidalgo, E., Gittins, J.R., Green, D.R.H., Tyrrell, T., Gibbs, S.J., von Dassow, P., Rehm, E., Armbrust, E.V. and Boessenkool, K.P. (2008) Phytoplankton calcification in a high-CO2 world. Science 320, 336–340.Google Scholar
Iwai, T. and Nishida, S. (1976) The distribution of modern coccolithophores in the North Pacific. News of the Osaka Micropaleontologists 5, 1–11.Google Scholar
Jordan, R.W. (2011) Coccolithophores. In Schaechter, M. (ed.) Eukaryotic microbes. San Diego, CA: Academic Press, pp. 235–247.Google Scholar
Komuro, C., Narita, H., Imai, K., Nojiri, Y. and Jordan, R.W. (2005) Microplankton assemblages at Station KNOT in the subarctic western Pacific, 1999–2000. Deep-Sea Research Part II 52, 2206–2217.Google Scholar
Konno, S. and Jordan, R.W. (2007) An emended terminology for the Parmales (Chrysophyceae). Phycologia 46, 612–616.CrossRefGoogle Scholar
Konno, S. and Jordan, R.W. (2012) Parmales. In Oren A. and Pettis G.S. (eds) Encyclopedia of life sciences. Chichester: John Wiley & Sons, pp. 1–9. doi: 10.1002/9780470015902.a0023691.Google Scholar
Konno, S., Ohira, R., Komuro, C., Harada, N. and Jordan, R.W. (2007) Six new taxa of subarctic Parmales (Chrysophyceae). Journal of Nannoplankton Research 29, 108–128.CrossRefGoogle Scholar
Kosman, C.A., Thomsen, H.A. and Østergaard, J.B. (1993) Parmales (Chrysophyceae) from Mexican, Californian, Baltic, Arctic and Antarctic waters with the description of a new subspecies and several new forms. Phycologia 32, 116–128.Google Scholar
Lepš, J. and Šmilauer, P. (2003) Multivariate analysis of ecological data using CANOCO. Cambridge: Cambridge University Press, pp. 1–269.Google Scholar
Longhurst, A.R. (2007) Ecological geography of the sea, 2nd edition. San Diego, CA: Academic Press, pp. 1–542.Google Scholar
Luan, Q., Liu, S., Zhou, F. and Wang, J. (2016) Living coccolithophore assemblages in the Yellow and East China Seas in response to physical processes during fall 2013. Marine Micropaleontology 123, 29–40.Google Scholar
Marchant, H.J. and McEldowney, A. (1986) Nanoplanktonic siliceous cysts from Antarctica are algae. Marine Biology 92, 53–57.Google Scholar
McIntyre, A. and Bé, A.W.H. (1967) Modern coccolithophoridae of the Atlantic Ocean – I. placoliths and cyrtoliths. Deep Sea Research 14, 561–597.Google Scholar
Montes-Hugo, M., Doney, S.C., Ducklow, H.W., Fraser, W., Martinson, D., Stammerjohn, S.E. and Schofield, O. (2009) Recent changes in phytoplankton communities associated with rapid regional climate change along the western Antarctic Peninsula. Science 323, 1470–1473.Google Scholar
Nishida, S. (1979) Atlas of Pacific nanoplanktons. News of the Osaka Micropaleontologists, Special Paper 3, 1–31.Google Scholar
Nishida, S. (1986) Nannoplankton flora in the Southern Ocean, with special reference to siliceous varieties. Memoirs of the National Institute for Polar Research, Special Issue 40, 56–68.Google Scholar
O'Brien, C.J., Vogt, M. and Gruber, N. (2016) Global coccolithophore diversity: drivers and future change. Progress in Oceanography 140, 27–42.Google Scholar
Park, J.-Y., Kug, J.-S., Bader, J., Rolph, R. and Kwon, M. (2015) Amplified arctic warming by phytoplankton under greenhouse warming. Proceedings of the National Academy of Sciences USA 112, 5921–5926.Google Scholar
Peña-Izquierdo, J., Pelegrí, J.L., Pastor, M.V., Castellanos, P., Emelianov, M., Gasser, M., Salvador, J. and Vázquez-Domínguez, E. (2012) The continental slope current system between Cape Verde and the Canary Islands. Scientia Marina 76, 65–78.Google Scholar
Peterson, R.G. and Stramma, L. (1991) Upper-level circulation in the South Atlantic Ocean. Progress in Oceanography 26, 1–73.Google Scholar
Riebesell, U., Zondervan, I., Rost, B., Tortell, P.D., Zeebe, R.E. and Morel, F.M.M. (2000) Reduced calcification of marine plankton in response to increased atmospheric CO2. Nature 407, 364–367.CrossRefGoogle ScholarPubMed
Rost, B. and Riebesell, U. (2004) Coccolithophores and the biological pump: response to environmental changes. In Thierstein, H.R. and Young, J.R. (eds) Coccolithophores – from molecular processes to global impact. Berlin: Springer, pp. 99–127.Google Scholar
Rousseaux, C.S. and Gregg, W.W. (2014) Interannual variation in phytoplankton primary production at a global scale. Remote Sensing 6, 1–19.CrossRefGoogle Scholar
Shannon, C.E. and Weaver, W. (1949) The mathematical theory of communication. Urbana: University of Illinois Press, pp. 1–117.Google Scholar
Silver, M.W., Mitchell, J.G. and Ringo, D.L. (1980) Siliceous nanoplankton. II. Newly discovered cysts and abundant choanoflagellates from the Weddell Sea, Antarctica. Marine Biology 58, 211–217.CrossRefGoogle Scholar
Takahashi, E., Watanabe, K. and Satoh, H. (1986) Siliceous cysts from Kita-no-seto Strait, north of Syowa Station, Antarctica. Memoirs of the National Institute for Polar Research, Special Issue 40, 84–95.Google Scholar
Tanimoto, M., Aizawa, C. and Jordan, R.W. (2003) Assemblages of living microplankton from the subarctic North Pacific and Bering Sea during July–August 1999. Courier Forschungsinstitut Senckenberg 244, 83–103.Google Scholar
Thomas, M.K., Kremer, C.T., Klausmeier, C.A. and Litchman, E. (2012) A global pattern of thermal adaptation in marine phytoplankton. Science 338, 1085–1088.Google Scholar
Turner, J., Lu, H., White, I., King, J.C., Phillips, T., Hosking, J.S., Bracegirdle, T.J., Marshall, G.J., Mulvaney, R. and Deb, P. (2016) Absence of 21st century warming on Antarctic Peninsula consistent with natural variability. Nature 535, 411–415.Google Scholar
Urban, J.L., McKenzie, C.H. and Deibel, D. (1993) Nannoplankton found in fecal pellets of macrozooplankton in coastal Newfoundland waters. Botanica Marina 36, 267–281.Google Scholar
Warton, D.I., Wright, I.J., Falster, D.S. and Westoby, M. (2006) Bivariate line-fitting methods for allometry. Biological Reviews 81, 259–291.Google Scholar
Waters, R.L., van den Enden, R. and Marchant, H.J. (2000) Summer microbial ecology off East Antarctica (80–150°E): protistan community structure and bacterial abundance. Deep-Sea Research Part II 47, 2401–2435.Google Scholar
Winter, A., Henderiks, J., Beaufort, L., Rickaby, R.E.M. and Brown, C.W. (2014) Poleward expansion of the coccolithophore Emiliania huxleyi. Journal of Plankton Research 36, 316–325.Google Scholar
Yamada, K., Yoshikawa, S., Ichinomiya, M., Kuwata, A., Kamiya, M. and Ohki, K. (2014) Effects of silicon-limitation on growth and morphology of Triparma laevis NIES-2565 (Parmales, Heterokontophyta). PLoS ONE 9, e103289.Google Scholar
Young, J.R., Geisen, M., Cros, L., Kleijne, A., Sprengel, C., Probert, I. and Østergaard, J. (2003) A guide to extant coccolithophore taxonomy. Journal of Nannoplankton Research, Special Issue 1, 1–125.Google Scholar
Zielinski, U. (1997) Parmales species (siliceous marine nanoplankton) in surface sediments of the Weddell Sea, Southern Ocean: indicators for sea-ice environment? Marine Micropaleontology 32, 387–395.Google Scholar
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