Skip to main content
SpringerLink
Log in

Super-Species in the calcareous plankton

  • Chapter
Coccolithophores

Summary

The most successful groups of pelagic protists in the modern Ocean have evolved convergent phenotypic traits, including the presence of hard skeletons enclosing the cell. These micro-skeletons – tests, coccoliths, frustules, theca – have accumulated kilometers of deep-sea sediments since the Jurassic, the most complete and continuous fossil record widely used for reconstructing Earth systems dynamics and microbial evolution. The use of the traditional morphological species concepts in those groups indicates that the relatively few species living at a given time have huge, often circum-global biogeographic distributions, and commonly last for many million years in the sediment record, which contrasts with the hectic biological pace of life occurring in the oceanic water masses, leading to one of the highest organismic turnover that any ecosystem sustains. Here we review all recent genetic data on coccolithophore and foraminifer biodiversity. In both groups, the sequencing of various genes shows that the morphological ‘species’ are in fact monophyletic assemblages of sibling species which diverged several million years ago according to molecular clock calculations. Furthermore the sibling species within a morphological entity may systematically occupy restricted geographic or temporal allopatric subdivisions of the total ecological range attributed to the traditional morphospecies. They display also stable and subtle – despite million years of genetic isolation – morphological differences that have been previously overlooked or interpreted as ecophenotypic variations. Obviously, various selective forces related to life in the marine planktic realm impose a strong stabilizing selection on pelagic organisms that maintains “optimal” phenotypes through the origination and possibly extinction of sibling species. We propose that this mode of evolution is characteristic of most marine planktic taxa, including metazoans, and we introduce a concept of ‘planktic super-species’ to describe these constrained morphological monophyletic entities that include several sibling species adapted to different ecological niches. Two different evolutionary models displaying different degrees of complexity in the spatio-temporal disconnection between morphological and genetic/ecologic differentiations are discussed in the frame of the existing morphometric and DNA data sets. The design of experimental protocols at the boundary between molecular phylogenetics and micropa-leontology will be a necessary condition to test which of our models reflect the real world. This will be also a crucial step to reveal the full potential of microfossil applications in paleoecology and stratigraphy, and to understand, at the level at which adaptation and selection operate, how pelagic biodiversity reacted to climatic changes in the past oceans and how it may react to the severe warming events projected in the near future.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Antoine D, André JM, Morel A (1996) Oceanic primary production 2. Estimation at global scale from satellite (coastal zone color scanner) chlorophyll. Global Biogeochem Cy 10: 57–69

    Article  Google Scholar 

  • Arnold AJ, Parker WC (1999) Biogeography of planktic foraminifera. In: Gupta BKS (ed) Modern foraminifera. Kluwer academic publishers, Dordrecht, Boston, London, pp 103–122

    Google Scholar 

  • Bé AWH (1977) An ecological, Zoogeographic and taxonomic review of recent planktic foraminifera. In: Ramsay ATS (ed) Oceanic micropaleontology. vol. 1. Academic Press, London, pp 1–100

    Google Scholar 

  • Beaufort L, Heussner S (2001) Seasonal dynamics of calcareous nannoplankton on a West European continental margin: the Bay of Biscay. Mar Micropaleontol 43 (1–2): 27–55

    Article  Google Scholar 

  • Berggren WA, Kent DV, Aubry MP, Hardenbol J (1995) Geochronology, Time Scales and Global Stratigraphic Correlations. SEPM, Spec Pub n°54 of the Society for Sediment Geol, Tulsa, USA, pp 386

    Google Scholar 

  • Bijma J, Hemleben C, Huber BT, Erlenkeuser H, Kroon D (1998) Experimental determination of the ontogenetic stable isotope variability in two morphotypes of Globigerinella siphonifera (d’Orbigny). Mar Micropaleontol 35: 141–160

    Article  Google Scholar 

  • Bolli HM, Saunders JB, Perch-Nielsen K (1985) Plankton stratigraphy. Cambridge University Press, Cambridge

    Google Scholar 

  • Bollmann J (1997) Morphology and biogeography of Gephyrocapsa coccoliths in Holocene sediments. Mar Micropaleontol 29: 319–350

    Article  Google Scholar 

  • Bollmann J, Baumann KH, Thierstein HR (1998): Global dominance of Gephyrocapsa coccoliths in Late Pleistocene: Selective dissolution, evolution, or global environmental change? Paleoceanography 13: 517–529

    Article  Google Scholar 

  • Bollmann J, Henderiks J, Brabec B (2002) Global calibration of Gephyrocapsa coccolith abundances in Holocene sediments for paleotemperature assessment. Paleoceanography 3 (17): 1–9

    Google Scholar 

  • Brand LE (1982) Genetic variability and spatial patterns of genetic differentiation in the reproductive rates of the marine coccolithophores Emiliania huxleyi and Gephyrocapsa oceanica. Limnol Oceanogr 27: 236–245

    Article  Google Scholar 

  • Bucklin A, La Jeunesse T, Curry TC, Wallinga EJ, Garrison K (1996) Molecular diversity of the copepod, Nannocalanus minor: genetic evidence of species and population structure in the North Atlantic Ocean. J Mar Res 54: 285–310

    Article  Google Scholar 

  • Cifelli R (1969) Radiation of the Cenozoic planktic foraminifera. Syst Zoology 18: 154–168

    Article  Google Scholar 

  • CLIMAP Project Members (1981) Seasonal reconstructions of the Earth’s surface at the last glacial maximum. Geol Soc Amer Map and Chart Series. MC-36

    Google Scholar 

  • Darling KF, Kroon D, Wade CM, Leigh AJ (1996) Molecular phylogeny of the planktic foraminifera. J Foram Res 26: 324–330

    Article  Google Scholar 

  • Darling KF, Wade CM, Kroon D, Leigh Brown A (1997) Planktic foraminiferal molecular evolution and their polyphyletic origins from benthic taxa. Mar Micropaleontol 30: 51–266

    Article  Google Scholar 

  • Darling KF, Wade CM, Kroon D, Leigh Brown AJ, Bijma J (1999) The diversity and distribution of modern planktic foraminiferal small subunit ribosomal RNA genotypes and their potential as tracers of present and past ocean circulations. Paleoceanography 14(1): 3–12

    Article  Google Scholar 

  • Darling KF, Wade CM, Stewart IA, Kroon D, Dingle R, Brown AJ (2000) Molecular evidence for genetic mixing of Arctic and Antarctic subpolar populations of planktic foraminifers. Nature 405 (6782): 43–47

    Article  Google Scholar 

  • Darling KF, Kucera M, Wade C, Kroon D, Pudsey C, Dingle R, Brinkmeyer R, Stangeew E, Bauch D (2001) Unravelling the genetic relationships between the bipolar high latitude populations of the planktic foraminifer Neogloboquadrina pachyderma sin. Proceedings of the ICP VII meeting, Hokkaido, Japan

    Google Scholar 

  • Darling KF, Kucera M, Wade CM, Von Langen P, Pak D (2003) Seasonal distribution of genetic types of planktic foraminifer morphospecies in the Santa Barbara Channel and its paleoceanographic implications. Paleoceanography 18 (2): 1032

    Article  Google Scholar 

  • de Vargas C (2000) Molecular evolution in planktic foraminifera. Doctoral Thesis n° 3182, University of Geneva, pp 1–194

    Google Scholar 

  • de Vargas C, Pawlowski J (1998) Molecular versus taxonomic rates of evolution in planktic foraminifera. Mol Phylogenet Evol 9: 463–469

    Article  Google Scholar 

  • de Vargas C, Zaninetti L, Hilbrecht H, Pawlowski J (1997) Phylogeny and rates of molecular evolution of planktic foraminifera: S SU rDNA sequences compared to the fossil record. J Mol Evol 45: 285–294

    Article  Google Scholar 

  • de Vargas C, Norris R, Zaninetti L, Gibb SW, Pawlowski J (1999) Molecular evidence of cryptic speciation in planktic foraminifera and their relation to oceanic provinces. Proc Nat Acad Sci USA 96: 2864–2868

    Article  Google Scholar 

  • de Vargas C, Renaud S, Hilbrecht H, Pawlowski J (2001) Pleistocene adaptive radiation in Globorotalia truncatulinoides: genetic, morphological and environmental evidence. Paleobiology 27: 104–125

    Article  Google Scholar 

  • de Vargas C, Bonzon M, Rees N, Pawlowski J, Zaninetti L (2002) A molecular approach to biodiversity and ecology in the planktic foraminifera Globigerinella siphonifera (d’Orbigny). Mar Micropaleontol 45: 101–116

    Article  Google Scholar 

  • de Vargas C, Norris R, Palumbi S (submitted) Shell and DNA analyses from single foraminifer: a new perspective on the pelagic fossil record. Deep-Sea Res

    Google Scholar 

  • Duboule D, Wilkins AS (1998)The evolution of ‘bricolage’. Trends Genet 14 (2): 54–59

    Article  Google Scholar 

  • Fischer G, Wefer G (1999) Use of proxies in paleoceanography. Springer Verlag, Berlin

    Book  Google Scholar 

  • Fleminger A (1972) Habitat patterns among epiplanktic calanoid copepods. Trans Amer Micros Soc 91 (1): 86–87

    Google Scholar 

  • Fuhrman JA, Campbell L (1998) Microbial biodiversity. Nature 393: 410–411

    Article  Google Scholar 

  • Geisen M, Billard C, Broerse ATC, Cros L, Probert I, Young JR (2002) Life-cycle associations involving pairs of holococcolithophorid species: Intraspecific variation or cryptic speciation? Euro J Phycol 37: 531–550

    Article  Google Scholar 

  • Haq BU, Boersma A (1998) Introduction to marine micropaleontology. Elsevier, N.Y.

    Google Scholar 

  • Healy-Williams N, Ehrlich R, Williams DF (1985) Morphometric and stable isotopic evidence for subpopulations of Globorotalia truncatulinoides. J Foram Res 15: 242–253

    Article  Google Scholar 

  • Hemleben C, Spindler M, Anderson OR (1989) Modern Planktic Foraminifera. Springer-Verlag, New York, Berlin, Heidelberg, London, Paris, Tokyo, pp 363

    Book  Google Scholar 

  • Hey J (2001) The mind of the species problem. Trends Ecol Evol 16 (7): 326–329

    Article  Google Scholar 

  • Hilbrecht H (1996) Extant planktic foraminifera and the physical environment in the Atlantic and Indian Oceans – Mitteilungen aus dem Geologischen Institut der Eidgen. Technischen Hochschule und der Universität Zürich, Neue Folge. No. 300, pp 93

    Google Scholar 

  • Huber BT, Bijma J, Darling K (1997) Cryptic speciation in the living planktic foraminifer Globigerinella siphonifera (d’Orbigny). Paleobiology 23: 33–62

    Google Scholar 

  • Jordan RW, Green JC (1994) A check-list of the extant Haptophyta of the world. J Mar Biol Assoc UK. Plymouth 74: 149–174

    Article  Google Scholar 

  • Jordan RW, Kleijne A (1994) A classification system for living coccolithophores. In: Winter A, Siesser WG (eds) Coccolithophores. Cambridge Univ. Press, Cambridge, pp 83–105

    Google Scholar 

  • Jordan RW, Kleijne A, Heimdal BR, Green JC (1995) A glossary of the extant Haptophyta of the world. J Mar Biol Assoc UK. Plymouth 75: 769–814

    Article  Google Scholar 

  • Kennett JP (1968) Globorotalia truncatulinoides as a paleo-oceanographic index. Science 159: 1461–1463

    Article  Google Scholar 

  • Kennett JP (1970) Pleistocene paleoclimates and foraminiferal biostratigraphy in subant-arctic deep-sea cores. Deep-Sea Res 17: 125–140

    Google Scholar 

  • Kennett JP (1976) Phenotypic variation in some recent and late Cenozoic planktic foraminifera. In: Hedley RH, Adams CG (eds) Foraminifera. Vol. 2. Academic Press, London, pp 111–170

    Google Scholar 

  • Kennett JP, Srinivasan MS (1983) Neogene Planktic Foraminifera, a Phylogenetic Atlas. Hutchinson Ross Publishing Company, Stroudsburg, Pennsylvania, pp 265

    Google Scholar 

  • Knappertsbusch M (1990) Geographic distribution of modern coccolithophorids in the Mediterranean Sea and morphological evolution of Calcidiscus leptoporus. PhD Dissertation ETH No. 9169

    Google Scholar 

  • Knappertsbusch M (2000) Morphologic evolution of the coccolithophorid Calcidiscus leptoporus from the early Miocene to recent. J Paleont 74: 712–730

    Article  Google Scholar 

  • Knappertsbusch M, Cortés MY, Thierstein HR (1997) Morphologic variability of the coccolithophorid Calcidiscus leptoporus in the plankton, surface sediments and from the Early Pleistocene. Mar Micropaleontol 30: 293–317

    Article  Google Scholar 

  • Knowlton N (1993) Sibling species in the Sea. Ann Rev Ecol Sys 24: 189–216

    Article  Google Scholar 

  • Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobi-ologia 420: 73–90

    Article  Google Scholar 

  • Kucera M, Darling KF (2001) Cryptic species of planktic foraminifera: their effect on palaeoceanographic reconstructions. Phil Trans R Soc Lond A 360: 695–718

    Google Scholar 

  • Kucera M, Kennett JP (2002) Causes and consequences of a middle Pleistocene origin of the modern planktic foraminifer Neogloboquadrina pachyderma sinistral. Geology 30: 539–542

    Article  Google Scholar 

  • Lazarus D, Hilbrecht H, Spencer-Cervato C, Thierstein H (1995) Sympatric speciation and phyletic change in Globorotalia truncatulinoides. Paleobiology 21: 28–51

    Google Scholar 

  • Li WKW (2002) Macroecological patterns of phytoplankton in the northwestern North Atlantic Ocean. Nature 419: 154–157

    Article  Google Scholar 

  • Mayr E (1971) Populations, species and evolution. Belknap press, Harvard University press, Cambridge, 453 pp

    Google Scholar 

  • Medlin LK, Lange M, Edvardsen B, Larsen A (2001) Cosmopolitan haptophyte flagellates and their genetic links. In: Leadbeater BSC, Green OG, John C (eds) The Flagellates. Unity, diversity and evolution. 1. Taylor & Francis Ltd: 288–308

    Google Scholar 

  • Milliman J (1993) Production and accumulation of calcium carbonates in the ocean: budget of a nonsteady state. Global Biogeochem Cy 7: 927–957

    Article  Google Scholar 

  • Miya M, Nishida M (1997) Speciation in the open ocean. Nature 389: 803–804

    Article  Google Scholar 

  • Moreira D, Lopez-Garcia P (2002) The molecular ecology of microbial eukaryotes unveils a hidden world. Trends Microbiol 10 (1): 31–38

    Article  Google Scholar 

  • Nanney DL (1982) Genes and phenes in Tetrahymena. Bioscience 32: 783–788

    Article  Google Scholar 

  • Norris R (1991) Biased extinction and evolutionary trends. Paleobiology 17 (4): 388–399

    Google Scholar 

  • Pharr RB Jr, Williams DF (1987) Shape changes in Globorotalia truncatulinoides as a function of ontogeny and paleobiogeography in the southern ocean. Mar Micropaleontol 12: 343–355

    Article  Google Scholar 

  • Renaud S, Klaas C (2001) Seasonal variations in the morphology of the coccolithophore Calcidiscus leptoporus off Bermuda (N. Atlantic). J Plankton Res 23: 779–795

    Article  Google Scholar 

  • Renaud S, Ziveri P, Broerse ATC (2002) Geographical and seasonal differences in morphology and dynamics of the coccolithophore Calcidiscus leptoporus. Mar Micro-paleontol 46: 363–385

    Article  Google Scholar 

  • Roth PH (1994) Distribution of coccoliths in oceanic sediments. In: Winter A, Siesser WG (eds) Coccolithophores. Cambridge Univ. Press, Cambridge, pp 199–218

    Google Scholar 

  • Sáez AG, Probert I, Quinn P, Young JR, Geisen M, Medlin LK (2003) Pseudocryptic spe-ciation in coccolithophores. Proc Nat Acad Sci USA 100 (12): 6893–7418

    Article  Google Scholar 

  • Schmidt D, Thierstein HR, Bollmann J (submitted) The evolutionary history of size variation of planktic foraminiferal assemblages in the Cenozoic. Palaeogeogr Palaeocl

    Google Scholar 

  • Scholin CA, Hallegraeff GM, Anderson DM (1995) Molecular evolution of the Alexan-drium tamarense ‘species complex’ (Dinophyceae): dispersal in the North and West Pacific regions. Phycologia 34: 472–485

    Article  Google Scholar 

  • Smetacek V (2001) A watery arms race. Nature 411 (6839): 745

    Article  Google Scholar 

  • Spencer-Cervato C (1999) The Cenozoic deep sea microfossil record: explorations of the DSDP/ODP sample set using the Neptune database. Paleontologica Electronica 2/2

    Google Scholar 

  • Spencer-Cervato C, Thierstein HR (1997) Fist appearance of Globorotalia truncatulinoides: cladocenensis and immigration. Mar Micropaleontol 30: 267–291

    Article  Google Scholar 

  • Steinberg DK, Carlson DA, Bates NR, Johnson RH, Michaels AF, Knap AH (2001) Overview of the US JGOFS Bermuda Atlantic Time-series Study (BATS): a decade-scale look at ocean biology and biogeochemistry. Deep-Sea Res 48: 1405–1447

    Article  Google Scholar 

  • Stewart IA (2000) The molecular evolution of planktic foraminifera and its implications for the fossil record. PhD Thesis, University of Edinburgh, UK

    Google Scholar 

  • Stewart IA, Darling KF, Kroon D, Wade CM, Troelstra SR (2001) Genotypic variability in subarctic Atlantic planktic foraminifera. Mar Micropaleontol 43: 143–153

    Article  Google Scholar 

  • Tappan H, Loeblich AR (1973) Evolution of the Oceanic Plankton. Earth-Science Rev 9: 207–240

    Article  Google Scholar 

  • Van der Spoel S, Heyman PP (1983) A comparative Atlas of Zooplankton. Springer-Verlag, New York, Berlin, Heidelberg, London, Paris, Tokyo, pp 186

    Google Scholar 

  • Vaulot D, Marie D, Olson RJ, Chisholm SW (1995) Growth of Prochlorococcus, a photo-synthetic prokaryote, in the equatorial Pacific Ocean. Science 268: 1480–1482

    Article  Google Scholar 

  • Verity PG, Smetacek V (1996) Organism life cycles, predation, and the structure of the marine pelagic ecosystems. Mar Ecol Prog Series 130: 277–293

    Article  Google Scholar 

  • Westbroek P, Van Hinte JE, Brummer GJ, Veldhuis M, Brownlee C, Green JC, Harris R, Heimdal BR (1994) Emiliania huxleyi as a key to biosphere-geosphere interactions. In: Green JC, Leadbeater BSC (eds) The haptophyte algae. Systematics Association Spec. Vol. 51, Clarendon Press, Oxford, pp 321–334

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Marine and Coastal Sciences, IMCS Rutgers University, New Brunswick, New Jersey, USA

    Colomban de Vargas

  2. Department of Biological Sciences, Imperial College at Silwood Park, Buckhurst Road, Ascot Berks, SL5 7PY, England

    Alberto G. Sáez

  3. Alfred Wegener Institute, Institute for Polar and Marine Research, Am Handelshafen 12, Bremerhaven, Germany

    Linda K. Medlin

  4. Geologisches Institut, ETHZ, Sonneggstrasse 5, CH-8092, Zürich, Switzerland

    Hans R. Thierstein

Authors
  1. Colomban de Vargas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alberto G. Sáez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Linda K. Medlin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hans R. Thierstein
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Geological Institute, ETH-Zentrum, 8092, Zürich, Switzerland

    Hans R. Thierstein

  2. Department of Palaeontology, The Natural History Museum, Cromwell Road, SW7 5BD, London, UK

    Jeremy R. Young

Rights and permissions

Reprints and permissions

Copyright information

© 2004 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

de Vargas, C., Sáez, A.G., Medlin, L.K., Thierstein, H.R. (2004). Super-Species in the calcareous plankton. In: Thierstein, H.R., Young, J.R. (eds) Coccolithophores. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-06278-4_11

Download citation

  • DOI: https://doi.org/10.1007/978-3-662-06278-4_11

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-06016-8

  • Online ISBN: 978-3-662-06278-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation