Warming will affect phytoplankton differently: Evidence through a mechanistic approach

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1724, 2011, Pages 3534-3543

  Huertas Emma, I ^a   Rouco, Mónica ^b   López Rodas, Victoria ^b   Costas, Eduardo ^b  

^a INSTITUTO DE CIENCIAS MARINAS DE ANDALUCÍA   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Climate change; Genetic adaptation; Phytoplankton; Ratchet technique; Warming

Indexed keywords

ADAPTATION; AQUATIC COMMUNITY; BIOGEOCHEMICAL CYCLE; BIOMECHANICS; COHORT ANALYSIS; GLOBAL WARMING; MICROSTRUCTURE; NET PRIMARY PRODUCTION; PHYTOPLANKTON; VULNERABILITY;

EID: 80054884391     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.0160     Document Type: Article

References (54)

1. Barnett, T. P., Pierce, D.W., AchutaRao, K. M., Gleckler, P. J., Santer, B. D., Gregory, J. M. & Washington, W. M. 2005 Penetration of human-induced warming into the world's oceans. Science 309, 284-287. (doi:10.1126/science.1112418)
2. Doney, S. C., Fabry, V. F., Feely, R. A. & Kleyplas, J. A. 2009 Ocean acidification: the other CO2 problem. Ann. Rev. Mar. Sci. 1, 169-192. (doi:10.1146/annurev. marine.010908.163834)
3. IPCC. 2007 Summary for policymakers. In Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor & H. L. Miller), pp. 7-22. Cambridge, UK: Cambridge University Press.
4. Trenberth, K. E., Jones, P. D., Ambenje, P., Bojariu, R., Easterling, D. et al. 2007 Observations: surface and atmospheric climate change. In Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor & H. L. Miller), pp. 235-336. Cambridge, UK: Cambridge University Press.
5. Hansen, J., Sato, M., Ruedy, R., Lo, K., Lea, D. V. & Medina-Elizade, M. 2006 Global temperature change. Proc. Natl Acad. Sci. USA 103, 14288-14293. (doi:10. 1073/pnas.0606291103)
6. Belkin, I. 2009 Rapid warming of large marine ecosystems. Prog. Oceanogr. 81, 207-213. (doi:10.1016/j.pocean.2009.04.011)
7. Meehl, G. A. et al. 2007 In Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor & H. L. Miller), pp. 748-845. Cambridge, UK: Cambridge University Press.
8. Magnuson, J. J., Webster, K. E., Assel, R. A., Bowser, C. J. & Dillon, P. J. 1997 Potential effects of climate changes on aquatic systems: Laurentian great lakes and Precambrian shield region. Hydrol. Process. 11, 825-871. (doi:10.1002/(SICI)1099-1085(19970630)11:8,825::AIDHYP509.3.0.CO;2-G)
9. Behrenfeld, M. J. et al. 2006 Climate-driven trends in contemporary ocean productivity. Nature 444, 752-755. (doi:10.1038/nature05317)
10. Cermeño, P., Dutkiewicz, S., Harris, R. P., Follows, M., Schofield, O. & Falkowski, P. G. 2008 The role of nutricline depth in regulating the ocean carbon cycle. Proc. Natl Acad. Sci. USA 105, 20344-20349. (doi:10.1073/pnas.0811302106)
11. Jöhnk, K. D., Huisman, J., Sharples, J., Sommeijer, B., Visser, P. M. & Stroom, J. M. 2008 Summer heatwaves promote blooms of harmful cyanobacteria. Glob. Change Biol. 14, 495-512. (doi:10.1111/j.1365-2486.2007.01510.x)
12. Muren, U., Berglund, J., Samuelsson, K. & Andersson, A. 2005 Potential effects of elevated sea-water temperature on pelagic food webs. Hydrobiologia 545, 153-166. (doi:10.1007/s10750-005-2742-4)
13. O'Connor, M.I., Piehler, M.F., Leech, D. M., Anton, A. & Bruno, J. F. 2009 Warming and resource availability shift food web structure and metabolism. PLoS Biol. 7, e1000178. (doi:10.1371/journal.pbio.1000178)
14. Hofmann, G. E. & Todgham, A. E. 2010 Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annu. Rev. Physiol. 72, 127-145. (doi:10.1146/annurev-physiol-021909-135900)
15. Strecker, A. L., Cobb, T. P. & Vinebrooke, R. D. 2004 Effects of experimental greenhouse warming on phytoplankton and zooplankton communities in fishless alpine ponds. Limnol. Oceanogr. 49, 1182-1190. (doi:10.4319/lo.2004.49.4.1182)
16. Daufresne, M., Lengfellnera, K. & Sommer, U. 2009 Global warming benefits the small in aquatic ecosystems. Proc. Natl Acad. Sci. USA 106, 12788-12793. (doi:10.1073/pnas.0902080106)
17. Moran, X. A., Lopez-Urrutia, A., Calvo-Diaz, A. & Li, W. K. W. 2010 Increasing importance of small phytoplankton in a warmer ocean. Glob. Change Biol. 16, 1137-1144. (doi:10.1111/j.1365-2486.2009.01960.x)
18. Finkel, Z. V., Beardall, J., Flynn, K. J., Quigg, A., Rees, T. A. V. & Raven, J. A. 2010 Phytoplankton in a changing world: cell size and elemental stoichiometry. J. Plankton Res. 32, 119-137. (doi:10.1093/plankt/fbp098)
19. Fogg, G. E. 2001 Algal adaptation to stress-some general remarks. In Algal adaptation to environmental stresses: physiological, biochemical and molecular mechanisms (eds L. C. Rai & J. P. Gaur), pp. 1-20. Berlin, Germany: Springer.
20. Sniegowski, P. D. & Lenski, R. E. 1995 Mutation and adaptation: the directed mutation controversy in evolutionary perspective. Annu. Rev. Ecol. Evol. Syst. 26, 553-578. (doi:10.1146/annurev.es.26.110195.003005)
21. Reboud, X., Majerus, N., Gasquez, J. & Powles, S. 2007 Chlamydomonas reinhardtii as a model system for proactive herbicide resistance evolution research. Biol. J. Linn. Soc. 91, 257-266. (doi:10.1111/j.1095-8312.2007.00787.x)
22. Huertas, I. E., Rouco, M., López-Rodas, V. & Costas, E. 2010 Estimating the capability of different phytoplankton groups to adapt to contamination: herbicides will affect phytoplankton species differently. New Phytol. 188, 478-487. (doi:10.1111/j.1469-8137.2010.03370.x)
23. Costas, E., Flores-Moya, A., Perdigones, N., Maneiro, E., Blanco, J. L., García, M. E. & López-Rodas, V. 2007 How eukaryotic algae can adapt to the Spain's Rio Tinto: a neo-Darwinian proposal for rapid adaptation to an extremely hostile ecosystem. New Phytol. 175, 334-339. (doi:10.1111/j.1469-8137.2007.02095.x)
24. López-Rodas, V., Flores-Moya, A., Maneiro, E., Perdigones, N., Marva, F., García, M. E. & Costas, E. 2007 Resistance to glyphosate in the cyanobacterium Microcystis aeruginosa as result of pre-selective mutations. Evol. Ecol. 21, 535-547. (doi:10.1007/s10682-006-9134-8)
25. López-Rodas, V., Marvá, F., Costas, E. & Flores-Moya, A. 2008 Microalgal adaptation to a stressful environment (acidic, metal-rich mine waters) could be due to selection of pre-selective mutants originating in non-extreme environments. Environ. Exp. Bot. 64, 43-48. (doi:10.1016/j.envexpbot.2008.01.001)
26. López-Rodas, V., Marvá, F., Rouco, M., Costas, E. & Flores-Moya, A. 2008 Adaptation of the chlorophycean Dictyosphaerium chlorelloides to stressful acidic, mine metal-rich waters as result of pre-selective mutations. Chemosphere 72, 703-707. (doi:10.1016/j.chemosphere.2008.04.009)
27. Marvá, F., López-Rodas, V., Rouco, M., Navarro, M., Toro, F. J., Costas, E. & Flores-Moya, A. 2010 Adaptation of green microalgae to the herbicides simazine and diquat as result of presselective mutations. Aquat. Toxicol. 96, 130-134. (doi:10.1016/j.aquatox.2009.10.009)
28. Novick, A. & Szilard, L. 1950 Chemostat on spontaneous mutations of bacteria. Proc. Natl Acad. Sci. USA 36, 708-719. (doi:10.1073/pnas.36.12.708)
29. Sniegowski, P. D. 2005 Linking mutation to adaptation: overcoming stress at the spa. New Phytol. 166, 360-362. (doi:10.1111/j.1469-8137.2005.01419.x)
30. Flores-Moya, A., Costas, E. & Lopez-Rodas, V. 2008 Roles of adaptation, chance and history in the evolution of the dinoflagellate Prorocentrum triestinum. Naturwissenschaften 95, 697-703. (doi:10.1007/s00114-008-0372-1)
31. Gould, S. J. 1989 Wonderful life: the Burguess shale and the nature of history. New York, NY: Norton.
32. Travisano, M. J. A., Mongold, J. A., Bennett, A. F. & Lenski, R. E. 1995 Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267, 87-90. (doi:10.1126/science.7809610)
33. Rouco, M., López-Rodas, V., Flores-Moya, A. & Costas, E. In press. Evolutionary changes in growth rate and toxin production in the cyanobacterium Microcystis aeruginosa under a scenario of eutrophication and temperature increase. Microb. Ecol. (doi:10.1007/s00248-011-9804-0)
34. Nicklisch, A., Shatwell, T. & Köhler, J. 2008 Analysis and modelling of the interactive effects of temperature and light on phytoplankton growth and relevance for the spring bloom. J. Plankton Res. 30, 75-91. (doi:10.1093/plankt/fbm099)
35. Suzuki, Y. & Takahashi, M. 1995 Growth responses of several diatoms isolated from various environments to temperature. J. Phycol. 31, 880-888. (doi:10.1111/j.0022-3646.1995.00880.x)
36. Butterwick, C., Heaney, S. I. & Talling, J. F. 2005 Diversity in the influence of temperature on the growth rates of freshwater algae, and its ecological relevance. Freshw. Biol. 50, 291-300. (doi:10.1111/j.1365-2427.2004.01317.x)
37. Hays, G. C., Richardson, A. J. & Robinson, C. 2005 Climate change and marine plankton. Trends Ecol. Evol. 20, 337-344. (doi:10.1016/j.tree.2005.03.004)
38. Cox, P. A. et al. 2005 Diverse taxa of cyanobacteria produce b-N-methylamino-L-alanine, a neurotoxic amino acid. Proc. Natl Acad. Sci. USA 102, 5074-5078. (doi:10.1073/pnas.0501526102)
39. Staehr, P. A. & Birkeland, M. J. 2006 Temperature acclimation of growth, photosynthesis and respiration in two mesophilic phytoplankton species. Phycologia 45, 648-656. (doi:10.2216/06-04.1)
40. Sánchez, J. F., Fernández-Sevilla, J. M., Acién, F. G., Cerón, M. C., Pérez-Parra, J. & Molina-Grima, E. 2008 Biomass and lutein productivity of Scenedesmus almeriensis: influence of irradiance, dilution rate and temperature. Appl. Microbiol. Biotechnol. 9, 719-729. (doi:10.1007/s00253-008-1494-2)
41. Costas, E., Flores-Moya, A. & López-Rodas, V. 2008 Rapid adaptation of phytoplankters to geothermal waters is achieved by single mutations: were extreme environments 'Noah's arks' for photosynthesizers during the Neoproterozoic 'snowball Earth'? New Phytol. 180, 922-932. (doi:10.1111/j.1469-8137.2008.02620.x)
42. Iglesias-Prieto, R., Matta, J. S., Robins, W. A. & Trench, R.K. 1992 Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc. Natl Acad. Sci. USA 89, 10302-10305. (doi:10.1073/pnas.89.21.10302)
43. Strychara, K. B., Coates, M., Sammarco, P. W., Pivab, T. J. & Scott, P. T. 2005 Loss of Symbiodinium from bleached soft corals Sarcophyton ehrenbergi, Sinularia sp. and Xenia sp. J. Exp. Mar. Biol. Ecol. 320, 159-177. (doi:10.1016/j.jembe.2004.12.039)
44. Loram, J. E., Trapido-Rosenthal, H. G. & Douglas, A. E. 2007 Functional significance of genetically different symbiotic algae Symbiodinium in a coral reef symbiosis. Mol. Ecol. 16, 4849-4857. (doi:10.1111/j.1365-294X.2007.03491.x)
45. Takahashi, S., Whitney, S., Itoh, S., Maruyama, T. & Badger, M. 2008 Heat stress causes inhibition of the de novo synthesis of antenna proteins and photobleaching in cultured Symbiodinium. Proc. Natl Acad. Sci. USA 105, 4203-4208. (doi:10.1073/pnas. 0708554105)
46. Takahashi, S., Whitney, S. & Badger, M. 2009 Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc. Natl Acad. Sci. USA 106, 3237-3242. (doi:10.1073/pnas.0808363106)
47. Berkelmans, R. & van Oppen, M. J. H. 2006 The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era of climate change. Proc. R. Soc. B 273, 2305-2312. (doi:10.1098/rspb.2006.3567)
48. Affan, A., Leel, J. B., Kim, J. T., Choi, Y. C., Kim, J. M. & Myoung, J. G. 2007 Seasonal dynamics of phytoplankton and environmental factors around the Chagwi-do off the West Coast of Jeju Island, Korea. Ocean Sci. J. 42, 117-127. (doi:10.1007/BF03020879)
49. Hernández-Becerril, D. U., Cortés-Altamirano, R. & Alonso, R. 2000 The dinoflagellate genus Prorocentrum along the coasts of the Mexican Pacific. Hydrobiologia 418, 111-121. (doi:10.1023/A:1003806719515)
50. Winter, A., Jordan, R. W. & Roth, P. H. 1994 Biogeography of living coccolithophores in ocean waters. In Coccolithophores (eds A. Winter & W. G. Siesser), pp. 161-177. Cambridge, UK: Cambridge University Press.
51. Smyth, T. J., Tyrrell, T. & Tarrant, B. 2004 Time series of coccolithophore activity in the Barents Sea, from twenty years of satellite imagery. Geophys. Res. Lett. 31, L11302. (doi:10.1029/2004GL019735)
52. Sorrosa, J. M., Satoh, M. & Shiraiwa, Y. 2005 Low temperature stimulates cell enlargement and intracellular calcification of coccolithophorids. Mar. Biotechnol. 7, 128-133. (doi:10.1007/s10126-004-0478-1)
53. Langer, G., Gussonem, N., Nehrke, G., Riebesell, U., Eisenhauer, A. & Thoms, S. 2007 Calcium isotope fractionation during coccolith formation in Emiliania huxleyi: independence of growth and calcification rate. Geochem. Geophys. Geosyst. 8, Q05007. (doi:10.1029/2006GC001422)
54. Cloern, J.E. & Dufford, R. 2005 Phytoplankton community ecology: principles applied in San Francisco Bay. Mar. Ecol. Prog. Ser. 285, 11-28. (doi:10.3354/meps285011)