Among the planktonic dinoflagellates, the species-rich genus Neoceratium has particularly remarkable features that include its easily recognizable outline and large size. This ubiquitous genus shows consistent presence in all plankton samples and has been a model for numerous studies since the end of the 19th century. It has already been described as a good candidate to monitor water masses and describe ocean circulation. We argue that the sensitivity displayed by Neoceratium to water temperature also makes it relevant as an indicator of ocean warming. The advantages and interests of using Neoceratium species to monitor climate change on a large scale are reassessed in view of recent advances in understanding their biology and ecology.
References
[1]
Balech, E. El genero Protoperidinium Bergh, 1881 (Peridinium Ehrenberg, 1831, partim). In Rev. Mus. Argent. Cienc. Nat. Bernardino Rivadavia Inst. Nac. Invest. Cienc. Nat.; 1974; Volume 4, pp. 1–79. (in Spanish).
[2]
Gómez, F.; Moreira, D.; López-García, P. Neoceratium gen. nov., a new genus for all marine species currently assigned to Ceratium (Dinophyceae). Protist 2010, 161, 35–54, doi:10.1016/j.protis.2009.06.004.
[3]
Sournia, A. Le genre Ceratium (péridinien planctonique) dans le Canal de Mozambique: Contribution à une révision mondiale. Vie Milieu A 1967, 18, 375–499. (in French).
[4]
Dodge, J.D.; Marshall, H.G. Biogeographic analysis of the armored planktonic dinoflagellate Ceratium in the North Atlantic and adjacent seas1. J. Phycol. 1994, 30, 905–922.
[5]
Gómez, F. A list of free-living dinoflagellate species in the world’s oceans. Acta Bot. Croat. 2005, 64, 129–212.
[6]
Müller, O.F. Animalcula Infusoria Fluviatilia et Marina: Quae Detexit, Systematice Descripsit et ad Vivum Delineari Curavit; Nicholae Molleri: Copenhagen, Denmark, 1786.
[7]
J？rgensen, E. Die Ceratien: Eine kurze Monographie der Gattung Ceratium Schrank. Int. Revue ges. Hydrobiol. Hydrogr. 1911, 4, 1–124, doi:10.1002/iroh.19110040102.
[8]
Sournia, A. Classe des Dinophycées. In Atlas du Phytoplancton Marin. (in French); Sournia, A., Ed.; Centre National de la Recherche Scientifique: Paris, France, 1986; pp. 26–98.
[9]
Sullivan, J.M.; Swift, E. Photoenhancement of bioluminescence capacity in natural and laboratory populations of the autotrophic dinoflagellate Ceratium fusus (Ehrenb.) Dujardin. J. Geophys. Res. 1995, 100, 6565–6574, doi:10.1029/94JC01511.
[10]
Latz, M.I.; Nauen, J.C.; Rohr, J. Bioluminescence response of four species of dinoflagellates to fully developed pipe flow. J. Plankton Res. 2004, 26, 1529–1546, doi:10.1093/plankt/fbh141.
[11]
Brokaw, C.J.; Wright, L. Bending waves of the posterior flagellum of Ceratium. Science 1963, 142, 1169–1170.
[12]
Sato, H.; Greuet, C.; Cachon, M.; Cosson, J. Analysis of the contraction of an organelle using its birefringency: The R-fibre of the Ceratium (Dinoflagellate) flagellum. Cell Biol. Int. 2004, 28, 387–396, doi:10.1016/j.cellbi.2004.03.007.
[13]
Elbr？chter, M. Population dynamics of Ceratium in coastal waters of the Kiel Bay. Oikos 1973, 15, 43–48.
[14]
Weiler, C.S.; Eppley, R.W. Temporal pattern of division in the dinoflagellate genus Ceratium and its application to the determination of growth rate. J. Exp. Mar. Biol. Ecol. 1979, 39, 1–24, doi:10.1016/0022-0981(79)90002-9.
[15]
Weiler, C.S. Population structure and in situ division rates of Ceratium in oligotrophic waters of the North Pacific central gyre. Limnol. Oceanogr. 1980, 25, 610–619, doi:10.4319/lo.1980.25.4.0610.
[16]
Pizay, M.D.; Lemée, R.; Simon, N.; Cras, A.L.; Laugier, J.P.; Dolan, J.R. Night and day morphologies in a planktonic dinoflagellate. Protist 2009, 160, 565–575, doi:10.1016/j.protis.2009.04.003.
[17]
Smalley, G.W.; Coats, D.W.; Adam, E.J. A new method using fluorescent microspheres to determine grazing on ciliates by the mixotrophic dinoflagellate Ceratium furca. Aquat. Microb. Ecol. 1999, 17, 167–179, doi:10.3354/ame017167.
[18]
Smalley, G.W.; Coats, D.W.; Stoecker, D.K. Feeding in the mixotrophic dinoflagellate Ceratium furca is influenced by intracellular nutrient concentrations. Mar. Ecol. Prog. Ser. 2003, 262, 137–151, doi:10.3354/meps262137.
[19]
Skovgaard, A.; Hansen, P.J.; Stoecker, D.K. Physiology of the mixotrophic dinoflagellate Fragilidium subglobosum. I. Effects of phagotrophy and irradiance on photosynthesis and carbon content. Mar. Ecol. Prog. Ser. 2000, 201, 129–136, doi:10.3354/meps201129.
[20]
Raine, R.; White, M.; Dodge, J.D. The summer distribution of net plankton dinoflagellates and their relation to water movements in the NE Atlantic Ocean, west of Ireland. J. Plankton Res. 2002, 24, 1131–1147, doi:10.1093/plankt/24.11.1131.
[21]
Ochoa, N.; Gómez, O. Dinoflagellates as indicators of water masses during El Ni？o, 1982–1983. J. Geophys. Res. Oceans 1987, 92, 14355–14367, doi:10.1029/JC092iC13p14355.
[22]
Sanchez, G.; Calienes, R.; Zuta, S. The 1997–98 El Nin？ and its effects on the coastal marine ecosystem off Peru. CalCOFI Rep. 2000, 41, 62–86.
[23]
Semina, H.J.; Levashova, S.S. The biogeography of tropical phytoplankton species in the Pacific Ocean. Int. Revue ges. Hydrobiol. Hydrogr. 1993, 78, 243–262, doi:10.1002/iroh.19930780210.
[24]
Dodge, J.D. Biogeography of the planktonic dinoflagellate Ceratium in the western Pacific. Korean J. Phycol. 1993, 8, 109–119.
[25]
Okolodkov, Y.B.; Dodge, J.D. Biodiversity and biogeography of planktonic dinoflagellates in the Arctic Ocean. J. Exp. Mar. Biol. Ecol. 1996, 202, 19–27, doi:10.1016/0022-0981(96)00028-7.
[26]
Dale, V.H.; Beyeler, S.C. Challenges in the development and use of ecological indicators. Ecol. Indic. 2001, 1, 3–10, doi:10.1016/S1470-160X(01)00003-6.
[27]
Tunin-Ley, A.; Labat, J.P.; Gasparini, S.; Mousseau, L.; Lemée, R. Annual cycle and diversity of species and infraspecific taxa of Ceratium (Dinophyceae) in the Ligurian Sea, northwest Mediterranean. J. Phycol. 2007, 43, 1149–1163, doi:10.1111/j.1529-8817.2007.00417.x.
[28]
Tunin-Ley, A.; Vaugelas, J.D.; Garcia, D.; Marro, S.; Lemée, R. A new collaborative web site to improve the accuracy of dinoflagellate identification: Focus on the morphologically-variable genus Neoceratium (Schrank) Gomez, Moreira et Lopez-Garcia. Cryptogam. Algol. 2012, 33, 399–404, doi:10.7872/crya.v33.iss4.2012.399.
[29]
Margalef, R. Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanol. Acta 1978, 1, 493–509.
[30]
Tunin-Ley, A.; Iba？ez, F.; Labat, J.P.; Zingone, A.; Lemée, R. Phytoplankton biodiversity and NW Mediterranean Sea warming: Changes in the dinoflagellate genus Ceratium in the 20th century. Mar. Ecol. Prog. Ser. 2009, 375, 85–99, doi:10.3354/meps07730.
[31]
Li, T.; Liu, S.; Huang, L.; Huang, H.; Lian, J.; Yan, Y.; Lin, S. Diatom to dinoflagellate shift in the summer phytoplankton community in a bay impacted by nuclear power plant thermal effluent. Mar. Ecol. Prog. Ser. 2011, 424, 75–85, doi:10.3354/meps08974.
[32]
Vázquez-Domínguez, E.; Vaqué, D.; Gasol, J.M. Temperature effects on the heterotrophic bacteria, heterotrophic nanoflagellates, and microbial top predators of the NW Mediterranean. Aquat. Microb. Ecol. 2012, 67, 107–121, doi:10.3354/ame01583.
[33]
Edwards, M.; Johns, D.G.; Leterme, S.C.; Svendsen, E.; Richardson, A.J. Regional climate change and harmful algal blooms in the northeast Atlantic. Limnol. Oceanogr. 2006, 51, 820–829, doi:10.4319/lo.2006.51.2.0820.
[34]
Edwards, M.; Richardson, A.J. Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 2004, 430, 881–884, doi:10.1038/nature02808.
[35]
Taylor, F.J. A preliminary annotated check list of dinoflagellates from New Zealand coastal waters. J. R. Soc. N. Z. 1974, 4, 193–201, doi:10.1080/03036758.1974.10426439.
[36]
Okolodkov, Y.B. A checklist of dinoflagellates recorded from the Russian Arctic seas. Sarsia 1998, 83, 267–292.
[37]
Gómez, F. Checklist of Mediterranean free-living dinoflagellates. Bot. Mar. 2003, 46, 215–242.
[38]
Gómez, F.; Boicenco, L. An annotated checklist of dinoflagellates in the Black Sea. Hydrobiologia 2004, 517, 43–59, doi:10.1023/B:HYDR.0000027336.05452.07.
[39]
Hoppenrath, M. A revised checklist of planktonic diatoms and dinoflagellates from Helgoland (North Sea, German Bight). Helgol. Mar. Res. 2004, 58, 243–251, doi:10.1007/s10152-004-0190-6.
[40]
Guilloux, L.; Rigaut Jalabert, F.; Jouenne, F.; Ristori, S.; Viprey, M.; Not, F.; Vaulot, D.; Simon, N. An annotated checklist of Marine Phytoplankton taxa at the SOMLIT-Astan time series off Roscoff (Western English Channel, France): Data collected from 2000 to 2010. Cah. Biol. Mar. 2013, 54, 247–256.
[41]
Nagasoe, S.; Kim, D.I.; Shimasaki, Y.; Oshima, Y.; Yamaguchi, M.; Honjo, T. Effects of temperature, salinity and irradiance on the growth of the red tide dinoflagellate Gyrodinium instriatum Freudenthal et Lee. Harmful Algae 2006, 5, 20–25, doi:10.1016/j.hal.2005.06.001.
[42]
Baek, S.H.; Shimode, S.; Kikuchi, T. Growth of dinoflagellates, Ceratium furca and Ceratium fusus in Sagami Bay, Japan: The role of temperature, light intensity and photoperiod. Harmful Algae 2008, 7, 163–173, doi:10.1016/j.hal.2007.06.006.
[43]
Xu, N.; Duan, S.; Li, A.; Zhang, C.; Cai, Z.; Hu, Z. Effects of temperature, salinity and irradiance on the growth of the harmful dinoflagellate Prorocentrum donghaiense Lu. Harmful Algae 2010, 9, 13–17, doi:10.1016/j.hal.2009.06.002.
[44]
Garmendia, M.; Borja, A.; Franco, J.; Revilla, M. Phytoplankton composition indicators for the assessment of eutrophication in marine waters: Present state and challenges within the European directives. Mar. Pollut. Bull. 2013, 66, pp. 7–16. Available online: http://dx.doi.org/10.1016/j.marpolbul.2012.10.005 (accessed on 15 January 2013).
[45]
Devlin, M.; Best, M.; Coates, D.; Bresnan, E.; O’Boyle, S.; Park, R.; Silke, J.; Cusack, C.; Skeats, J. Establishing boundary classes for the classification of UK marine waters using phytoplankton communities. Mar. Pollut. Bull. 2007, 55, 91–103, doi:10.1016/j.marpolbul.2006.09.018.
[46]
Domingues, R.B.; Barbosa, A.; Galv？o, H. Constraints on the use of phytoplankton as a biological quality element within the Water Framework Directive in Portuguese waters. Mar. Pollut. Bull. 2008, 56, 1389–1395, doi:10.1016/j.marpolbul.2008.05.006.
[47]
Henriksen, P. Reference conditions for phytoplankton at Danish Water Framework Directive intercalibration sites. Hydrobiologia 2009, 629, 255–262, doi:10.1007/s10750-009-9767-z.
[48]
Hays, G.C.; Richardson, A.J.; Robinson, C. Climate change and marine plankton. Trends Ecol. Evol. 2005, 20, 337–344, doi:10.1016/j.tree.2005.03.004.
[49]
Beaugrand, G.; Reid, P.C.; Ibanez, F.; Lindley, J.A.; Edwards, M. Reorganisation of North Atlantic marine copepod biodiversity and climate. Science 2002, 296, 1692–1694, doi:10.1126/science.1071329.
[50]
Hinder, S.L.; Manning, J.E.; Gravenor, M.B.; Edwards, M.; Walne, A.W.; Burkill, P.H.; Hays, G.C. Long-term changes in abundance and distribution of microzooplankton in the NE Atlantic and North Sea. J. Plankton Res. 2012, 34, 83–91, doi:10.1093/plankt/fbr087.
[51]
Philippart, C.J.; Anadón, R.; Danovaro, R.; Dippner, J.W.; Drinkwater, K.F.; Hawkins, S.J.; Oguz, T.; O’Sullivan, G.; Reid, P.C. Impacts of climate change on European marine ecosystems: Observations, expectations and indicators. J. Exp. Mar. Biol. Ecol. 2011, 400, 52–69, doi:10.1016/j.jembe.2011.02.023.
Sieracki, C.K.; Sieracki, M.E.; Yentsch, C.S. An imaging-in-flow system for automated analysis of marine microplankton. Mar. Ecol. Prog. Ser. 1998, 168, 285–296, doi:10.3354/meps168285.
[54]
Karsenti, E. Towards an “Oceans Systems Biology”. Mol. Syst. Biol. 2012. Available online: http://www.nature.com/msb/journal/v8/n1/full/msb20128.html (accessed on 27 March 2012).
