Probing diversity in the plankton: using patterns in Tintinnids (planktonic marine ciliates) to identify mechanisms

  • John R. Dolan
  • Rodolphe Lemée
  • Stéphane Gasparini
  • Laure Mousseau
  • Céline Heyndrickx
Part of the Developments in Hydrobiology book series (DIHY, volume 183)


In diversity research, the use of survey data appears to have declined in favour of experimental or modeling approaches because direct relationships are difficult to demonstrate. Here we show that use of field data can yield information concerning the mechanisms governing diversity. First, we establish that tintinnids display a global latitudinal pattern of diversity similar to other pelagic organisms; species numbers appear to peak between 20° and 30° north or south. This common large scale spatial trend has been attributed to the gradient in water column structure across the global ocean. We then examine the generality of a relationship between planktonic diversity and water column structure by considering data from the Mediterranean Sea, in which water column structure changes seasonally. Among populations of foraminifera, tintinnids, and the dinoflagellates of the genus Ceratium, we compare data from trans-Mediterranean sampling conducted at different times and monthly changes in species richness at single sites. We find that water column structure alone appears to be a poor predictor of temporal changes in diversity. Lastly, we present an example of temporal changes in tintinnid diversity based on data from an oceanographic sampling station in the N. W. Mediterranean where resources, as chlorophyll, appear distinctly unrelated to changes in water column structure. We show that short-tem temporal changes in diversity (week to week shifts) can be related to changes in chlorophyll concentration. We conclude that in tintinnids diversity can be directly linked to characteristics of food resources.

Key words

biogeography biodiversity zooplankton Mediterranean latitudinal gradient phytoplankton foraminifera 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Agatha, S., M. C. Strûder-Kypke, A. Beran & D. H. Lynn, 2005. Pelagostrobilidium neptuni (Montagnes and Taylor, 1994) and Strombidium biarmatum nov. spec. (Ciliophora, Oligotrichea): phylogenetic position inferred from morphology, ontogenesis, and gene sequence data. European Journal of Protistolology 41: 65–83.CrossRefGoogle Scholar
  2. Angel, M. V., 1993. Biodiversity of the Pelagic Ocean. Conservation Biology 7: 760–772.CrossRefGoogle Scholar
  3. Balech, E., 1959. Tintinnoinea del Mediterraneo. Trabajo Instituto Espanol de Oceanografia 28: 1–88.Google Scholar
  4. Bethoux, J. P., 1989. Oxygen consumption, new production, vertical advection and environmental evolution in the Mediterranean Sea. Deep-Sea Research 36: 769–781.CrossRefGoogle Scholar
  5. de Barrio Cao, M. S., 1992. Abundance and species composition of Tintinnina (Ciliophora) in Bahia Blanca Estuary, Argentina. Estuarine Coastal Shelf Science 34: 295–303.CrossRefGoogle Scholar
  6. Bolotovskoy, D., S. M. Vivequin & N. R. Swanberg, 1991. Vertical distribution of tintinnids and associated microplankton in the upper layer of the Barents Sea. Sarsia 76: 141–151.Google Scholar
  7. Buckling, A., R. Kassen, G. Bell & P. B. Rainey, 2000. Disturbance and diversity in experimental microcosms. Nature 408: 961–964.PubMedCrossRefGoogle Scholar
  8. Bustillo-Guzman, J., H. Claustre & J.-C. Marty, 1995. Specific phytoplankton signatures and their relationship with hydrographic conditions in the coastal northwestern Mediterranean Sea. Marine Ecology Progress Series 124: 247–258.Google Scholar
  9. Campbell, A. S., 1942. The Oceanic Tintinnoina of the Plankton Gathered During the Last Cruise of the Carnegie. Carnegie Institution of Washington, Publication 537, Washington D.C.Google Scholar
  10. Capriulo, G. M. & E. J. Carpenter, 1983. Abundance, species composition and feeding impact of tintinnid micro-zooplankton in central Long Island Sound. Marine Ecology Progress Series 10: 277–288.Google Scholar
  11. Cariou, J.-B., J. R. Dolan & S. Dallot, 1999. A preliminary study of tintinnid diversity in the NW Mediterranean Sea. Journal of Plankton Research 21: 1065–1075.CrossRefGoogle Scholar
  12. Caron, D. A. & N. R. Swanberg, 1990. The ecology of planktonic sarcodines. Reviews in Aquatic Sciences 3: 147–180.Google Scholar
  13. Caron, D. A., A. F. Michaels, N. R. Swanberg & F. A. Howes, 1995. Primary productivity by symbiont-bearing planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda. Journal of Plankton Research 17:103–129.CrossRefGoogle Scholar
  14. Darling, K. F., C. M. Wade, I. A. Stewart, D. Kroon, R. Dingle & A. I. Brown, 2000. Molecular evidence for genetic mixing of artic and antarctic subpolar populations of planktonic foraminifers. Nature 405: 23–24.CrossRefGoogle Scholar
  15. Darling K. F., M. Kucera, C. J. Pudsey & C. M. Wade, 2004. Molecular evidence links cryptic diversification in polar planktonic protists to Quaternary climate dynamics. Proceeding of the National Academy of Sciences USA 101: 7657–7662.CrossRefGoogle Scholar
  16. Darwin, C., 1859. On the Origin of Species by Means of Natural Selection. Facsimile edition. 1964. Harvard University Press, Boston, USA.Google Scholar
  17. Dodson, S. I., S. E. Arnott & K. L. Cottingham, 2000. The relationship in lake communities between primary productivity and species richness. Ecology 81: 2662–2679.CrossRefGoogle Scholar
  18. De Vargas, C., R. Norris, L. Zaninetti, S. W. Gibb, & J. Pawlowski, 1999. Molecular evidence of cryptic speciation in planktonic foraminifera and their relation to ocean provinces. Proceedings of the National Academy of Sciences USA 96: 2864–2868.CrossRefGoogle Scholar
  19. De Vargas, C., M. Bonzon, N. W. Tess, J. Pawlowski & L. Zaninetti, 2002. A molecular approach to biodiversity and biogeography in the planktonic foraminifera Globigerinella siphonifera (d’Orbigny). Marine Micropaleontology 45: 101–116.CrossRefGoogle Scholar
  20. Dolan, J. R., 2000. Tintinnid ciliate diversity in the Mediterranean Sea: longitudinal patterns related to water column structure in late spring-early summer. Aquatic Microbial Ecology 22: 20–30.Google Scholar
  21. Dolan, J. R., 2005. Marine ecology-different measures of biodiversity. Nature 433: E9 (Jan 27 2005).Google Scholar
  22. Dolan, J. R & C. L. Gallegos, 2001. Estuarine diversity of tintinnids (planktonic ciliates). Journal of Plankton Research 23: 1009–1027.CrossRefGoogle Scholar
  23. Dolan, J. R. & C. Marassé, 1995. Planktonic ciliate distribution relative to a deep chlorophyll maximum: Catalan Sea, N. W. Mediterrean, June 1993. Deep-Sea Research 42: 1965–1987.CrossRefGoogle Scholar
  24. Dolan, J. R., T. F. Thingstad, & F. Rassoulzadegan, 1995. Phosphate transfer between microbial size-fractions in Villefranche Bay (N.W.Mediterranean Sea) France in autumn 1992.Google Scholar
  25. Dolan, J. R., F. Vidussi & H. Claustre, 1999. Planktonic ciliates in the Mediterranean Sea: longitudinal trends. Deep-Sea Research I 46: 2025–2039.CrossRefGoogle Scholar
  26. Dolan, J. R., H. Claustre, F. Carlotti, S. Plounevez & T. Moutin, 2002. Microzooplankton diversity: relationships of tintinnid ciliates with resources, competitors and predators from the Atlantic coast of Morocco to the eastern Mediterranean. Deep-Sea Research 1(49): 1217–1232.Google Scholar
  27. Emmerson, M. C., M. Solan, C. Emes, D. M. Paterson & D. Raffaell, 2001. Consistent patterns and the idiosyncratic effects of biodiversity in marine ecosystems. Nature 411: 73–77.PubMedCrossRefGoogle Scholar
  28. Fenchel, T., G. F. Esteban & B. Finlay, 1997. Local vs. global diversity of microorganisms: cryptic diversity of ciliated protozoa. Oikos 80: 220–225.CrossRefGoogle Scholar
  29. Finlay, B. J., 2002. Global dispersal of free-living microbial eukaryote species. Science 296: 1061–1063.PubMedCrossRefGoogle Scholar
  30. Finlay, B. J. & G. F. Esteban, 2004. Ubiquitous dispersal of free-living microorganisms. In Bull, A. T. (ed.) Microbial Diversity and Bioprocessing. ASM Press, Washington D.C., USA: 216–224.Google Scholar
  31. Finlay, B. J., G. F. Esteban & T. Fenchel, 1998. Protozoan diversity: converging estimates of the global number of freeliving ciliate species. Protist 149: 29–37.Google Scholar
  32. Finlay, B. J., G. F. Esteban, J. L. Olmo & P. A. Tyler, 1999. Global distribution of free-living microbial species. Ecography 22: 138–144.CrossRefGoogle Scholar
  33. Garder, K. R., 1946. Tintinnoinea from the “Michael Sars” North Atlantic Deep-Sea Expedition, 1910. In Murray, J. & J. Hjort, Report on the Scientific Results of the “Michael Sars” North Atlantic Deep-Sea Expedition, 1910. Bergen Musuem, Bergen, Norway.Google Scholar
  34. Gaston, K. J., 2000. Global patterns in biodiversity. Nature 405: 220–227.PubMedCrossRefGoogle Scholar
  35. Gold, K. & E. A. Morales, 1975. Seasonal changes in lorica sizes and the species of Tinntinida in the New York Bight. Journal of Protozoology 22: 520–528.Google Scholar
  36. Gold, K. & E. A. Morales, 1977. Studies on the Tintinnida of Enewetak Atoll. Journal of Protozoology 24: 580–587.Google Scholar
  37. Hargraves, P. E., 1981. Seasonal variations of tintinnids (Ciliophora: Oligotrichida) in Narragansett Bay, Rhode Island. Journal of Plankton Research 3: 81–91.CrossRefGoogle Scholar
  38. Hedlin, B. P. & J. T. Staley, 2004. Microbial endemism and biogeography. In Bull, A. T. (ed.) Microbial Diversity and Bioprocessing. ASM Press, Washington D.C, pp. 225–231.Google Scholar
  39. Hedin, H., 1974. Tintinnids on the swedish west coast. Zoon 2: 123–133.Google Scholar
  40. Huisman, J. & J. F. Weissing, 1999. Biodiversity of plankton by species oscillations and chaos. Nature 402: 407–410.CrossRefGoogle Scholar
  41. Hulot, F. D., G. Lacroix, F. Lescher-Moutoué & M. Loreau, 2000. Functional diversity governs ecosystem response to nutrient enrichment. Nature 405: 340–344.PubMedCrossRefGoogle Scholar
  42. Hutchinson, G. E., 1961. The paradox of the plankton. American Naturalist 95: 137–145.CrossRefGoogle Scholar
  43. Irigoien, X., J. Huisman & R. P. Harris 2004. Global biodiversity patterns of marine phytoplankton and zooplankton. Nature 429: 863–867.PubMedCrossRefGoogle Scholar
  44. James, M. R. & J. A. Hall, 1995. Planktonic ciliated protozoa: their distribution and relationship to environmental variables in a marine coastal ecosystem. Journal of Plankton Research 17: 659–683.CrossRefGoogle Scholar
  45. Jensen, F. & B. W. Hansen, 2000. Ciliates and heterotrophic dinoflagellates in the marginal ice zone of the central Barents Sea during spring. Journal of the Marine Biological Association United Kingdom 18: 45–54.CrossRefGoogle Scholar
  46. Jörgensen, E., 1924. Mediterranean Tintinnidae. Report of the Danish Oceanographical Expeditions 1908-1910 to the Mediterranean and adjacent seas. Vol. II. Biology, No. 8, J.3 (Thor expedition), Copenhagen.Google Scholar
  47. Kassen, R., A. Buckling, G. Bell & P. B. Rainey, 2000. Diversity peaks at intermediate productivity in a laboratory microcosm. Nature 406: 508–512.PubMedCrossRefGoogle Scholar
  48. Kofoid, C. A. & A. S. Campbell, 1929. A conspectus of the marine and fresh-water ciliate belonging to the suborder tintinnoinea, with descriptions of new species principally from the Agassiz expedition to the eastern tropical Pacific 1904-1905. University of California Publications in Zoology 34: 1–403.Google Scholar
  49. Kofoid, C. A. & A. S. Campbell, 1939. The tintinnoinea of the eastern tropical Pacific. Bulletin of the Museum of Comparative Zoology of Harvard College 84: 1–473.Google Scholar
  50. Longhurst, A. R., 1985. Relationship between diversity and the vertical structure of the upper ocean. Deep-Sea Research 1(32): 1535–1570.CrossRefGoogle Scholar
  51. Loreau, M. & A. Hector, 2001. Partitioning selection and complementarity in biodiversity experiments. Nature 412: 72–76.PubMedCrossRefGoogle Scholar
  52. Lynn, D. H. & E. B. Small, 1997. A revised classification of the phylum Ciliophora Doflein, 1901. Revista de la Sociadad de la Historia Naturale de Mexico 47: 65–78.Google Scholar
  53. Margalel, R., 1957. Fitoplancton de las costas de Blanes (Gerona) de agosto de 1952 a junio de 1956. Investigaciones Pesqueras 8: 89–95.Google Scholar
  54. Margalef, R. & E. Morales, 1960. Fitoplancton de las costas de Blanes (Gerona) de julio de 1956 a junio de 1959. Investigaciones Pesqueras 16: 3–31.Google Scholar
  55. McGowan, J. A. & P. W. Walker, 1980. Structure in the copepod community of the North Pacific Central grye. Ecological Monographs 49: 195–226.CrossRefGoogle Scholar
  56. McGowan, J. A. & P. W. Walker, 1985. Dominance and diversity maintenance in an oceanic ecosystem. Ecological Monographs 55: 103–118.CrossRefGoogle Scholar
  57. Middlebrook, K., C. W. Emerson, J. C. Roff & D. H. Lynn, 1987. Distribution and abundance of tintinnids in the Quoddy region of the Bay of Fundy. Canadian Journal of Zoology 65: 594–601.Google Scholar
  58. Modigh, M. & S. Castaldo, 2002. Variability and persistence in tintinnid assemblages in a Mediterranean coastal site. Aquatic Microbial Ecology 28: 299–311.Google Scholar
  59. Modigh, M., S. Castalado, M. Saggiomi & I. Santarpia, 2003. Distribution of tintinnid species from 42_ N to 43_ S through the Indian Ocean. Hydrobiologia 503: 251–262.CrossRefGoogle Scholar
  60. Monti, M. & S. Fonda Umani, 1995. Tintinnids in Terra Nova Bay-Ross Sea during two austral summers (1987/88 and 1989/90). Acta Protozoologica 34: 193–201.Google Scholar
  61. Mostajir, B., J. R. Dolan & F. Rassoulzadegan, 1995. Seasonal variations of pico-and nano-detrital particles (DAPI Yellow Particles DYP) in the Ligurian Sea (NW Mediterranean). Aquatic Microbial Ecology 9: 267–277.Google Scholar
  62. Naeem, S., 2002. Ecosystem consequences of biodiversity loss: the evolution of a paradigm. Ecology 83: 1537–1552.CrossRefGoogle Scholar
  63. Naeem, S. & S. Li, 1998. Consumer species richness and autrophic biomass. Ecology 79: 2603–2615.CrossRefGoogle Scholar
  64. Naeem, S., D. R. Hahn & G. Schuurman, 2000. Producerdecomposer co-dependency influences biodiversity effects. Nature 403: 762–764.PubMedCrossRefGoogle Scholar
  65. Ottens, J. J. & A. J. Nederbragt, 1992. Planktic foraminferal diversity as an indicator of ocean environment. Marine Micropaleontology 19: 13–28.CrossRefGoogle Scholar
  66. Paranjape, M., 1987. Grazing by microzooplankton in the Eastern Canadian Arctic in summer 1983. Marine Ecology Progress Series 40: 239–246.Google Scholar
  67. Petz, W. & W. Foissner, 1992. Morphology and morphogenesis of Strobilidium caudatum (Fromentel), Meseres corlissi N. Sp., Halteria graninella(Müller), and Strombidium rehwaldi N. Sp., and a proposed phylogenetic system for oligotrich ciliates (Protozoa, Ciliophora). Journal of Protozoology 39: 159–176.Google Scholar
  68. Pierce, R. W. & J. T. Turner, 1994. Plankton studies in Buzzards Bay, Massachusetts, USA. IV. Tintinnids, 1987 to 1988. Marine Ecology Progress Series 112: 235–240.Google Scholar
  69. Pujol C. & C. Vergnaud Grazzini, 1995. Distribution patterns of live planktic foraminifers as related to regional hydrography and productive systems of the Mediterranean Sea. Marine Micropaleontology 25: 187–217.CrossRefGoogle Scholar
  70. Rassoulzadegan, F., 1979. Evolution annuelle des ciliés pélagiques en Méditerranée nord-occidentale. II. Cilés oligotriches. Tintinnides (Tintinnia). Investigaciones Pesqueras 43: 417–488.Google Scholar
  71. Rampi, L., 1948. Tinttinnoidi delle acque di San Remo. Bollettino di Pesca, di Pisciocoltura e di Idrobiologia 24: 5–11.Google Scholar
  72. Rogers, G. F., J. C. Roff & D. H. Lynn, 1981. Tintinnids of Chesterfield Inlet, Northwest Territories. Canadian Journal of Zoology 59: 2360–2364.Google Scholar
  73. Rutherford, S., S. D’Hondt & W. Prell, 1999. Environmental controls on the geographic distribution of zooplankton diversity. Nature 400: 749–752.CrossRefGoogle Scholar
  74. Sanders, R. W., 1987. Tintinnids and other microzooplankton-seasonal distributions and relationships to resources and hydrography in a Maine estuary. Journal of Plankton Research 9: 65–77.CrossRefGoogle Scholar
  75. Smetacek, V., 1996. Biodiversity and production in the water mass. In Hempel, G. (ed.) The Ocean and the Poles. Gustav Verlag, Jena: 207–216.Google Scholar
  76. Snoeyenbos-West, O. L. O., T. Salcedo, G. B. McManus & L. A. Katz, 2002. Insights into the diversity of choreotrich, oligotrich ciliates (Class: Spirotrichea) based on genealogical analyses of multiple loci. International Journal of Systematic and Evolutionary Microbiology 52: 1901–1913.PubMedCrossRefGoogle Scholar
  77. Silva, E. S., 1953. Estudos de plancton na Lagoa de Obidos II. Tintinnoinea. Revista de Faculdadae de Ciencias de Lisboa 2a Serie C 11: 97–116.Google Scholar
  78. Stoecker, D. K. & J. M. Capuzzo, 1990. Predation on protozoa: its importance to zooplankton. Journal of Plankton Research 12: 891–908.CrossRefGoogle Scholar
  79. Swanberg, N. R. & D. A. Caron, 1991. Patterns of sarcodine feeding in epipelagic oceanic plankton. Journal of Plankton Research 13: 287–312.CrossRefGoogle Scholar
  80. Taguchi, S., 1976. Microzooplankton and seston in Akkeshi Bay, Japan. Hydrobiologia 50: 195–204.CrossRefGoogle Scholar
  81. Thompson, G. A., 2004. Tintinnid diversity trends in the southwestern Atlantic Ocean (29-60_S). Aquatic Microbial Ecology 35: 93–130.Google Scholar
  82. Thompson, G. A., V. A. Alder, D. Boltovskoy & F. Brandini, 1999. Abundance and biogeography of tintinnids (Ciliophora) and associated microzooplankton in the Southwestern Atlantic Ocean. Journal of Plankton Research 21: 1265–1298.CrossRefGoogle Scholar
  83. Thompson, G. A., V. A. Alder & D. Boltovskoy, 2001. Tintinnids (ciliophora) and other net microzooplankton (>30 lm) in southw-western Atlantic Shelf break waters. P.S.Z.N. Marine Ecology 22: 343–355.CrossRefGoogle Scholar
  84. Travers, M., 1973. Le microplancton du Golfe de Marseille: variations de la composition systématique et de la densitédes populations. Tethys 5: 31–53.Google Scholar
  85. Turner, J. T., 1984. The Feeding Ecology of Some Zooplankters that are Important Prey Items of Larval Fish. NOAA Technical Report NMFS 7. NOAA, Washington D.C 28 pp.Google Scholar
  86. Venrick, E. L., 1990. Phytoplankton in an oligotrophic ocean: species structure and interannual variability. Ecology 71: 1547–1563.CrossRefGoogle Scholar
  87. Venrick, E. L., 1999. Phytoplankton species structure in the central North Pacific, 1973-1996: variability and persistence. Journal of Plankton Research 21: 1029–1042.CrossRefGoogle Scholar
  88. Vitiello, P., 1964. Contribution à l’étude des tintinnides de la baie d’Alger. Pelagos 2: 5–41.Google Scholar
  89. Wasik, A. & E. Mikolajczyk, 1990. Tintinnids near pack-ice between South Shetland and the South Orkney Islands (26 Dec. 1988-18 Jan. 1989). Acta Protozoologica 29: 229–244.Google Scholar
  90. Wilf, P., K. R. Johnson & B. T. Huber, 2003. Correlated terrestrial and marine evidence for global climate changes before mass extinction at the Cretaceous-Paleogene boundary. Proceedings of the National Academy of Sciences, USA 100: 599–604.CrossRefGoogle Scholar
  91. Williams, D. F. & W. C. Johnson II, 1975. Diversity of recent planktonic foraminifera in the southern Indian Ocean and late Pleistocene paleotemperatures. Quaternary Research 5: 237–250.CrossRefGoogle Scholar
  92. Worm, B., H. K. Lotze, H. Hillebrand & U. Sommer, 2002. Consumer versus resource control of species diversity and ecosystem functioning. Nature 417: 848–851.PubMedCrossRefGoogle Scholar
  93. Worm, B., H. K. Lotze & R. A. Myers, 2003. Predator diversity hotspots in the blue ocean. Proceedings of the National Academy of Sciences, USA 100: 9884–9888.CrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • John R. Dolan
    • 1
  • Rodolphe Lemée
    • 1
  • Stéphane Gasparini
    • 1
  • Laure Mousseau
    • 1
  • Céline Heyndrickx
    • 1
  1. 1.Marine Microbial Ecology GroupLaboratoire d’Océanographie de VillefrancheVillefranche-Sur-MerFrance

Personalised recommendations