Phytoplankton growth after a century of dormancy illuminates past resilience to catastrophic darkness

Nature Communications

Volumn 2, Issue 1, 2011, Pages

  Ribeiro, Sofia ^a,b,c   Berge, Terje ^a   Lundholm, Nina ^d   Andersen, Thorbjørn J ^a   Abrantes, Fátima ^b   Ellegaard, Marianne ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b LABORATÓRIO NACIONAL DE ENERGIA E GEOLOGIA   (Portugal)

^c UNIVERSITY OF LISBON   (Portugal)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAL GROWTH; ANIMAL CELL; ARTICLE; CELL DIVISION; DARKNESS; DINOFLAGELLATE; DORMANCY; ECOSYSTEM RESILIENCE; END CRETACEOUS MASS EXTINCTION; GERMINATION; ILLUMINATION; NONHUMAN; PHOTOSYNTHESIS; PHYTOPLANKTON; REST; SEASHORE; SEDIMENT; ECOSYSTEM; EVOLUTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; PHYSIOLOGY; RADIATION EXPOSURE;

BACILLARIOPHYTA; DINOPHYCEAE;

BIOLOGICAL EVOLUTION; DARKNESS; DINOFLAGELLIDA; ECOSYSTEM; LIGHT; PHYTOPLANKTON;

EID: 79956280795     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1314     Document Type: Article

References (46)

1. Krug, A. Z., Jablonski, D. & Valentine, J. W. Signature of the end-Cretaceous mass extinction in the modern biota. Science 323, 767-771 (2009).
2. Alvarez, L. W., Alvarez, W., Asaro, F. & Michel, H. V. Extraterrestrial cause for the Cretaceous-Tertiary extinction. Science 208, 1095-1108 (1980).
3. Schulte, P. et al. The Chicxulub asteroid impact and mass extinction at the Cretaceous-Paleogene boundary. Science 327, 1214-1218 (2010).
4. Toon, O. B., Turco, R. P. & Covey, C. Environmental perturbations caused by the impacts of asteroids and comets. Rev. Geophys. 35, 41-78 (1996).
5. Kring, D. The Chicxulub impact event and its environmental consequences at the Cretaceous-Tertiary boundary. Palaeogeogr. Palaeocl. Palaeoecol. 255, 4-21 (2007). (Pubitemid 47531822)
6. Twittchett, R. J. The palaeoclimatology, palaeoecology and palaeoenvironmental analysis of mass extinction events. Palaeogeogr. Palaeocl. Palaeoecol. 232, 190-213 (2006).
7. Pollack, J. B., Toon, O. B., Ackerman, T. P. & McKay, C. P. Environmental effects of an impact-generated dust cloud: implications for the Cretaceous-Tertiary Extinctions. Science 219, 287-289 (1983).
8. Pope, K. O., Baines, K. H., Ocampo, A. C. & Ivanov, B. A. Energy, volatile production, and climatic effects of the Chicxulub Cretaceous/Tertiary impact. J. Geophys. Res. 102, 21645-21664 (1997). (Pubitemid 127683942)
9. McLeod, N. et al. The Cretaceous-Tertiary biotic transition. J. Geol. Soc. London 154, 265-292 (1997).
10. Pospichal, J. J. in The Cretaceous-Tertiary Event and Other Catastrophes in Earth History Vol. 307 (eds Ryder, G., Fastovsky, D. & Gartner, S.) (Geological Society of America Special Papers, 1988).
11. D'Hondt, S., Donaghay, P., Zachos, J. C., Luttenberg, D. & Lindinger, M. Organic carbon fluxes and ecological recovery from the Cretaceous-Tertiary mass extinction. Science 282, 276-279 (1998). (Pubitemid 28487195)
12. Harwood, D. M. in Geology and Palaeontology of Seymour Island, Antarctic Peninsula, Vol. 169 (eds Feldmann, R. M. & Woodburne, M. O.) 55-129 (Geological Society of America Memoirs, 1988).
13. Brinkhuis, H. & Zachariasse, W. J. Dinoflagellate cysts, sea level changes and planktonic foraminifers across the Cretaceous-Tertiary boundary at El Haria, northern Tunisia. Mar. Micropaleontol. 13, 153-191 (1988).
14. Willumsen, P. S. Palynodinium minus sp. nov., a new dinoflagellate from the Cretaceous-Paleogene boundary in New Zealand. Its significance and palaeoecology. Cretaceous Res. 27, 954-963 (2006). (Pubitemid 44762930)
15. Prauss, M. L. The K/Pg boundary at Brazos-River, Texas, USA-an approach by marine palynology. Palaeogeogr. Palaeocl. Palaeoecol. 283, 195-215 (2009).
16. Sepúlveda, J., Wendler, J. E., Summons, R. E. & Hinrichs, K.- U. Rapid resurgence of marine productivity after the Cretaceous-Paleogene mass extinction. Science 326, 129-132 (2009).
17. Jones, H. et al. Experiments on mixotrophic protists and catastrophic darkness. Astrobiology 9, 563-571 (2009).
18. Rintala, J.- M., Spilling, K. & Blomster, J. Temporary cyst enables long-term dark survival of Scrippsiella hangoei (Dinophyceae). Mar. Biol. 152, 57-62 (2007). (Pubitemid 47050958)
19. D'Hondt, S., Pilson, M. E. Q., Sigurdsson, H., Hanson, A. K. Jr. & Carey, S. Surface-water acidification and extinction at the Cretaceous-Tertiary boundary. Geology 22, 983-986 (1994).
20. Bown, P. Selective calcareous nannoplankton survivorship at the Cretaceous-Tertiary boundary. Geology 33, 653-656 (2005). (Pubitemid 41070709)
21. Kitchell, J. A., Clark, D. L. & Gombos, A. M. Jr. Biological selectivity to extinction: a link between background and mass extinction. Palaios 1, 504-511 (1986). (Pubitemid 17263884)
22. Knoll, A. H. Evolution and extinction in the marine realm: some constraints imposed by phytoplankton. Phil. Trans. R. Soc. Lond. B 325, 279-290 (1989).
23. Genovesi-Giunti, B., Laabir, A. & Vaquer, A. The benthic resting cyst: a key actor in harmful dinoflagellate blooms-a review. Vie. Milieu. 56, 327-337 (2006). (Pubitemid 46680746)
24. Hargraves, P. E. & French, F. W. in Survival Strategies of the Algae (ed. Fryxell, G. A.) 49-68 (Cambridge University Press, 1983).
25. Lewis, J., Harris, A. S. D., Jones, K. J. & Edmonds, R. L. Long-term survival of marine planktonic diatoms and dinoflagellates in stored sediment samples. J. Plankton Res. 21, 343-354 (1999). (Pubitemid 29332226)
26. Keafer, B. A., Buesseler, K. O. & Anderson, D. M. Burial of living dinoflagellate cysts in estuarine and nearshore sediments. Mar. Micropaleontol. 20, 147-161 (1992). (Pubitemid 23377924)
27. McQuoid, M. R., Godhe, A. & Nordberg, K. Viability of phytoplankton resting stages in the sediments of a coastal Swedish fjord. Eur. J. Phycol. 37, 191-201 (2002). (Pubitemid 34523147)
28. Mizushima, K. & Matsuoka, K. Vertical distribution and germination ability of Alexandrium spp. cysts (Dinophyceae) in the sediments collected from Kure Bay of the Seto Inland Sea, Japan. Phycol. Res. 52, 408-413 (2004). (Pubitemid 39569265)
29. Binder, B. J. & Anderson, D. M. Biochemical composition and metabolic activity of Scrippsiella trochoidea (Dinophyceae) resting cysts. J. Phycol. 26, 289-298 (1990).
30. Gottschling, M., Renner, S. S., Meier, K. J. S., Willems, H. & Keupp, H. Timing deep divergence events in calcareous dinoflagellates. J. Phycol. 44, 429-438 (2008). (Pubitemid 351548577)
31. Nordberg, K., Filipsson, H. L., Gustafsson, M., Harland, R. & Roos, P. Climate, hydrographic variations and marine benthic hypoxia in Koljö Fjord, Sweden. J. Sea Res. 46, 187-200 (2001). (Pubitemid 34082130)
32. Anderson, D. M., Taylor, C. D. & Armbrust, E. V. The effects of darkness and anaerobiosis on dinoflagellate cyst germination. Limnol. Oceanogr. 32, 340-351 (1987).
33. Mller, R. D., Sdrolias, M., Gaina, C., Steinberger, B. & Heine, C. Long-term sea level driven by ocean basin volume change. Science 319, 1357-1362 (2008). (Pubitemid 351354865)
34. Arthur, M. A. & Sageman, B. B. Marine black shales: depositional mechanisms and environments of ancient deposits. Annu. Rev. Earth Planet. Sci. 22, 499-551 (1994).
35. Kremp, A. Effects of cyst resuspension on germination and seeding of two bloom-forming dinoflagellates in the Baltic Sea. Mar. Ecol. Prog. Ser. 216, 57-66 (2001). (Pubitemid 32731486)
36. Härnström, K., Ellegaard, M., Andersen, T. J. & Godhe, A. Hundred years of genetic structure in a sediment revived diatom population. Proc. Natl Acad. Sci. USA 108, 4252-4257 (2011).
37. Fay, P. Viability of akinetes of the planktonic cyanobacterium Anabaena circinalis. Proc. R. Soc. Lond. B 234, 283-301 (1988).
38. Livingstone, D. & Jaworski, G. H. M. The viability of akinetes of blue-green algae recovered from the sediments of Rostherne Mere. Br. Phycol. J. 15, 357-364 (1980).
39. Antia, N. J. Effects of temperature on the darkness survival of marine microplanktonic algae. Microbial Ecol. 3, 41-54 (1976).
40. Medlin, L. K., Sáez, A. G. & Young, J. R. A molecular clock for coccolitophores and implications for selectivity of phytoplankton extinctions across the K/T boundary. Mar. Micropaleontol. 67, 69-86 (2008). (Pubitemid 351382090)
41. Kirchner, J. & Weil, A. Delayed biological recovery from extinctions throughout the fossil record. Nature 404, 177-180 (2000). (Pubitemid 30154483)
42. Darling, K. F., Thomas, E., Kasemann, S. A., Seears, H. A., Smart, C. W. & Wade, C. M. Surviving mass extinction by bridging the benthic/planktic divide. Proc. Natl Acad. Sci. USA 106, 12629-12633 (2009).
43. Appleby, P. G. in Tracking Environmental Change Using Lake Sediments (eds Last, W. M. & Smol, J. P.) 171-203 (Kluwer Academic Publishers, 2001).
44. Larsen, N. H., Moestrup, ø. & Pedersen, P. M. (eds) Scandinavian Culture Centre. Catalogue 1994. (Department of Biology, University of Copenhagen, 1994).
45. Hansen, P. J. Effect of high pH on the growth and survival of marine phytoplankton. Aquat. Microb. Ecol. 28, 279-288 (2002).
46. R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2011)