Misuse of the phytoplankton-zooplankton dichotomy: The need to assign organisms as mixotrophs within plankton functional types

Journal of Plankton Research

Volumn 35, Issue 1, 2013, Pages 3-11

  Flynn, Kevin J ^a   Stoecker, Diane K ^b   Mitra, Aditee ^a   Raven, John A ^c   Glibert, Patricia M ^b   Hansen, Per Juel ^e   Granéli, Edna ^d   Burkholder, Joann M ^f  

^a SWANSEA UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF MARYLAND CENTER FOR ENVIRONMENTAL SCIENCE   (United States)

^c SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^d LINNAEUS UNIVERSITY   (Sweden)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

^f NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Microzooplankton; Mixotroph; Model; Phytoplankton; Plankton functional type; Primary production; Secondary production

Indexed keywords

CLIMATE CHANGE; FUNCTIONAL GROUP; MICROPLANKTON; MIXOTROPHY; NUMERICAL MODEL; PHOTOAUTOTROPHY; PHOTOSYNTHESIS; PHYTOPLANKTON; PIGMENT; PRIMARY PRODUCTION; PROTIST; SECONDARY PRODUCTION; ZOOPLANKTON;

EUKARYOTA; PROTISTA;

EID: 84871965659     PISSN: 01427873     EISSN: 14643774     Source Type: Journal    
DOI: 10.1093/plankt/fbs062     Document Type: Article

References (78)

1. Aiken, J., Hardman-Mountford, N. J., Barlow, R. et al. (2008) Functional links between bioenergetics and bio-optical traits of phytoplankton taxonomic groups: an overarching hypothesis with applications for ocean colour remote sensing. J. Plankton Res., 30, 165-181.
2. Azam, F., Fenchel, T., Field, J. G. et al. (1983) The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser., 10, 257-263.
3. Baretta-Bekker, J. G., Baretta, J. W., Hansen, A. S. et al. (1998) An improved model of carbon and nutrient dynamics in the microbial food web in marine enclosures. Aquat Microbial Ecol., 14, 91-108.
4. Bell, E. M. and Laybourn-Parry, J. (2003) Mixotrophy in the Antarctic phytoflagellate, Pyramimonas pedicola (Chlorophyta: Prasinophyceae). J. Phycol., 39, 644-649.
5. Berge, T., Poulsen, L. K., Moldrup, M. et al. (2012) Marine microalgae attack and feed on metazoans. ISME J., 6, 1-11.
6. Berman, T. and Bronk, D. A. (2003) Dissolved organic nitrogen: a dynamic participant in aquatic ecosystems. Aquat. Microb. Ecol., 31, 273-305.
7. Bernard, C. and Rassoulzadegan, F. (1994) Seasonal variations of mixotrophic ciliates in the northwest Mediterranean Sea. Mar. Ecol. Prog. Ser., 108, 295-301.
8. Bhatti, S. and Colman, B. (2008) Inorganic carbon assimilation in some synurophyte algae. Physiol. Plant., 133, 33-40.
9. Burkholder, J. M., Glibert, P. M. and Skelton, H. M. (2008) Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae, 8, 77-93.
10. Calbet, A. and Landry, M. R. (2004) Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol. Oceanogr., 49, 51-57.
11. Calbet, A. and Saiz, E. (2005) The ciliate-copepod link in marine ecosystems. Aquat. Microb. Ecol., 38, 157-167.
12. Calderon-Saenz, E. and Schnetter, R. (1989) Morphology, biology and systematics of Cryptochlora perforata, a phagotrophic marine alga. Plant Syst. Evol., 163, 165-176.
13. Callieri, C., Caravati, E., Morabito, G. et al. (2006) The unicellular freshwater cyanobacterium Synechococcus and mixotrophic flagellates: evidence for a functional association in an oligotrophic, alpine lake. Freshwater Biol., 51, 263-273.
14. Caron, D. A., Michaels, A. F., Swanberg, N. R. et al. (1995) Primary productivity by symbiont-bearing planktonic sarcodines (Acantharia, Radiolaria, Foraminifera) in surface waters near Bermuda. J. Plankton Res., 17, 103-129.
15. Carvalho, W. F. and Granéli, E. (2006) Acidotropic probes and flow cytometry: a powerful combination for detecting phagotrophy in mixotrophic and heterotrophic protists. Aquat. Microb. Ecol., 44, 85-96.
16. Carvalho, W. F. and Granéli, E. (2010) Contribution of phagotrophy versus autotrophy to Prymnesium parvum growth under nitrogen and phosphorus sufficiency and deficiency. Harmful Algae, 9, 105-115.
17. Ciavatta, S., Torres, R., Saux-Picart, S. et al. (2011) Can ocean color assimilation improve biogeochemical hindcasts in shelf seas? J. Geophys Res. Ocean, 116, C12043. doi: 10.1029/2011JC007219.
18. Croft, M. T., Warren, M. J. and Smith, A. G. (2006) Algae need their vitamins. Eukaryotic Cell, 5, 1175-1183.
19. Cushing, D. H. (1975) Marine Ecology and Fisheries. Cambridge University Press, Cambridge, UK.
20. Droop, M. R. (1959) Water soluble compounds in the nutrition of Oxyrrhis marina. J. Mar. Biol. Assoc. UK, 38, 605-620.
21. Esteban, G. F., Fenchel, T. and Finlay, B. J. (2010) Mixotrophy in ciliates. Protist, 161, 621-641.
22. Falkowski, P. and Kiefer, D. A. (1985) Chlorophyll a fluorescence in phytoplankton: relationship to photosynthesis and biomass. J. Plankton Res., 7, 715-731.
23. Fasham, M. J. R. (1995) Variations in the seasonal cycle of biological production in subarctic oceans: a model sensitivity analysis. Deep-Sea Res. I, 42, 1111-1149.
24. Fasham, M. J. R., Ducklow, H. W. and McKelvie, S. M. (1990) A nitrogen-based model of plankton dynamics in the oceanic mixed layer. J. Mar. Res., 48, 591-639.
25. Fileman, E., Petropavlovsky, A. Y. and Harris, R. (2010) Grazing by the copepods Calanus helgolandicus and Acartia clausi on the protozooplankton community at station L4 in the Western English Channel. J. Plankton Res., 32, 709-724.
26. Flynn, K. J. (2006) Reply to Horizons Article "Plankton functional type modelling: running before we can walk" Anderson (2005): II. Putting trophic functionality into plankton functional types. J. Plankton Res., 28, 873-876.
27. Flynn, K. J. and Butler, I. (1986) Nitrogen sources for the growth of marine microalgae; role of dissolved free amino acids. Mar. Ecol. Prog. Ser., 34, 281-304.
28. Flynn, K. J. and Mitra, A. (2009) Building the "perfect beast": modelling mixotrophic plankton. J Plankton Res, 31, 965-992.
29. Gifford, D. J. and Caron, D. A. (2000) Sampling, preservation, enumeration and biomass of marine protozooplankton. In Harris, R. P., Wiebe, P. H., Lenz, J. et al. (eds), ICES Zooplankton Methodology Manual. Academic Press, San Diego, pp. 193-221.
30. Gisselson, L. A., Carlsson, P., Granéli, E. et al. (2002) Dinophysis blooms in the deep euphotic zone of the Baltic Sea: do they grow in the dark? Harmful Algae, 1, 401-418.
31. Glibert, P. M. and Burkholder, J. M. (2011) Eutrophication and HABs: strategies for nutrient uptake and growth outside the Redfield comfort zone. Chin. J. Ocean. Limnol., 29, 724-738.
32. Glibert, P. M., Burkholder, J. M., Kana, T. M. et al. (2009) Grazing by Karenia brevis on Synechococcus enhances their growth rate and may help to sustain blooms. Aquat. Microb. Ecol., 55, 17-30.
33. Glibert, P. M. and Legrand, C. (2006) The diverse nutrient strategies of HABs: focus on osmotrophy. In Graneli, E. and Turner, J. (eds), Ecology of Harmful Algae. Springer, Berlin, pp. 163-176.
34. Granéli, E., Edvardsen, B., Roelke, D. L. et al. (2012) The ecophysiology and bloom dynamics of Prymnesium spp. Harmful Algae, 14, 260-270.
35. Hammer, A. C. and Pitchford, J. W. (2005) The role of mixotrophy in plankton bloom dynamics, and consequences for productivity. ICES J. Mar. Sci., 62, 833-840.
36. Hansen, P. J. (2011) The role of photosynthesis and food uptake for the growth of marine mixotrophic dinoflagellates. J. Eukaryot. Microbiol., 58, 203-214.
37. Hansen, P. J. and Hjorth, M. (2002) Growth and grazing response of Chrysochomulina erecina (Prymnesiophyceae): the role of irradiance, prey concentration and pH. Mar. Biol., 141, 975-983.
38. Hansen, P. J., Moldrup, M., Tarangkoon, W. et al. (2012) Direct evidence for symbiont sequestration in the marine red tide ciliate Mesodinium rubrum. Aquat. Microb. Ecol., 66, 63-75.
39. Hartmann, M., Grob, C., Tarran, G. A. et al. (2012) Mixotrophic basis of Atlantic oligotrophic ecosystems. Proc. Natl. Acad. Sci. USA, doi: 10.1073/pnas.1118179109.
40. Jeong, H. J. (2011) Mixotrophy in the red tide algae raphidophytes. J. Eukaryot. Microbiol., 58, 215-222.
41. Jeong, H. J., Park, J. Y., Nho, J. H. et al. (2005b) Feeding by red-tide dinoflagellates on the cyanobacterium Synechococcus. Aquat. Microb. Ecol., 41, 131-143.
42. Jeong, H. J., Seong, K. A., Kang, N. S. et al. (2010a) Feeding by raphidophytes on the cyanobacterium Synechococcus. Aquat. Microb. Ecol., 58, 181-195.
43. Jeong, H. J., Shim, J. H., Park, J. S. et al. (1999) The feeding by the thecate mixotrophic dinoflagellate Fragilidium cf. mexicanum on red tide and toxic dinoflagellates. Mar. Ecol. Prog. Ser., 176, 263-277.
44. Jeong, H. J., Yoo, Y. D., Kim, J. S. et al. (2010b) Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean. Sci. J., 45, 65-91.
45. Jeong, H. J., Yoo, Y. D., Park, J. Y. et al. (2005a) Feeding by the phototrophic red-tide dinoflagellates: 5 species newly revealed and 6 species previously known to be mixotrophic. Aquat. Microb. Ecol., 40, 133-150.
46. Jiao, N., Herndl, G. J., Hansell, D. A. et al. (2010) Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat. Rev. Microbiol., 8, 593-599.
47. Jones, H. L. J. (1997) A classification of mixotrophic protists based on their behaviour. Freshwater Biol., 37, 35-43.
48. Jones, R. I. (1994) Mixotrophy in planktonic protists as a spectrum of nutritional strategies. Mar. Microb. Food Webs, 8, 87-96.
49. Kristiansen, J. (2005) The Golden Algae: A Biology of Chrysophyceae, Koletz Scientific Books, Keoneigestin, pp. 167.
50. Laybourn-Parry, J., Marshall, W. A. and Marchant, H. (2005) Flagellate nutritional versatility as a key to survival in two contrasting Antarctic saline lakes. Freshwater Ecol., 50, 830-838.
51. Lindehoff, E., Granéli, E. and Glibert, P. M. (2011) Nitrogen uptake kinetics of Prymnesium parvum (Haptophyte). Harmful Algae, 12, 70-76.
52. Lochte, K., Ducklow, H. W., Fasham, M. J. R. et al. (1993) Plankton succession and carbon cycling at 478N 208W during the JGOFS North Atlantic Bloom Experiment. Deep Sea Res. II, 40, 91-114.
53. Maranger, R., Bird, D. F. and Price, N. M. (1998) Iron acquisition by photosynthetic marine phytoplankton from ingested bacteria. Nature, 396, 248-251.
54. Miller, C. B. and Wheeler, P. A. (2010) Biological Oceanography, 2nd edn. John Wiley & Sons, Ltd., Hoboken, NJ, 464 pp.
55. Minnhagen, S., Kim, M., Salomon, P. S. et al. (2011) Active uptake of kleptoplastids by Dinophysis caudata from its ciliate prey Myrionecta rubra. Aquat. Microb. Ecol., 62, 99-108.
56. Mitra, A. and Flynn, K. J. (2010) Modelling mixotrophy in harmful algal blooms: more or less the sum of the parts? J. Mar. Syst., 83, 158-169.
57. Mulholland, M. R., Lee, C. and Glibert, P. M. (2003) Extracellular enzyme activity and uptake of carbon and nitrogen along an estuarine nutrient and salinity gradient. Mar. Ecol. Prog. Ser., 258, 3-17.
58. Park, M. G., Kim, M., Kim, S. et al. (2010) Does Dinophysis caudata (Dinophyceae) have permanent plastids? J. Phycol., 46, 236-242.
59. Perez, M. T., Dolan, J. R. and Fukai, W. (1997) Planktonic oligotrich ciliates in the NW Mediterranean: growth rates and consumption by copepods. Mar. Ecol. Prog. Ser., 155, 89-101.
60. Poulsen, L. K., Moldrup, M., Berge, T. et al. (2011) Feeding on fecal pellets - a new trophic role for dinoflagellates as detritivores. Mar. Ecol. Prog. Ser., 441, 65-77.
61. Raven, J. A., Beardall, J., Flynn, K. J. et al. (2009) Phagotrophy in the origins of photosynthesis in eukaryotes and as a complementary mode of nutrition in phototrophs: relation to Darwin's Insectivorous Plants. J. Exp. Bot., 60, 3975-3987.
62. Rokitta, S. D., de Nooijer, L. J., Trimborn, S. et al. (2011) Transcriptional analyses reveal differential gene expression patterns between the life cycle stages of Emiliania huxleyi (Haptophyta) and reflects specialization to different ecological niches. J. Phycol., 47, 829-838.
63. Sanchez-Puerta, M. V. and Delwiche, C. F. (2008) A hypothesis for plastid evolution in chromalveolates. J. Phycol., 44, 1097-1107.
64. Sanders, R. W. (1991) Mixotrophic protists in marine and fresh-water ecosystems. J. Protozool., 38, 76-81.
65. Sanders, R. W. (1992) Trophic strategies among heterotrophic flagellates. In Patterson, D. J. and Larsen, J. (eds), The Biology of Free-Living Heterotrophic Flagellates. Systematics Association Special Vol. 45. Clarendon Press, Oxford, pp. 21-38.
66. Sanders, R. W. (2011) Alternative nutritional strategies in Protists: symposium introduction and a review of freshwater protists that combine photosynthesis and heterotrophy. J. Eukaryot. Microbiol., 58, 181-184.
67. Sarmiento, J. L. and Gruber, N. (2006) Ocean Biogeochemical Dynamics. Princeton University Press, NJ, USA.
68. Smalley, G. W., Coats, D. W. and Stoecker, D. K. (2003) Feeding in the mixotrophic dinoflagellate Ceratium furca is influenced by intracellular nutrient concentrations. Mar. Ecol. Prog. Ser., 262, 137-151.
69. Steele, J. H., Thorpe, S. A. and Turekian, K. K. (eds) (2010) Marine Ecological Processes. Elsevier, Academic Press, London, pp. 642.
70. Stickney, H. L., Hood, R. R. and Stoecker, D. K. (2000) The impact of mixotrophy on planktonic marine ecosystems. Ecol. Model., 125, 203-230.
71. Stoecker, D., Li, A., Coats, D. W. et al. (1997) Mixotrophy in the dinoflagellate Prorocentrum minimum. Mar. Ecol. Prog. Ser., 15, 1-12.
72. Stoecker, D., Tillmann, U. and Granéli, E. (2006) Phagotrophy in harmful algae. In: Granéli, E. and Turner, J. (eds) Ecology of Harmful Algae, Series: Ecological Studies, Vol. 189, Springer Verlag, Heidelberg, pp 177-187.
73. Stoecker, D. A. (1998) Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. Eur. J Protistol, 34, 281-290.
74. Stoecker, D.K., Gustafson, D. E. and Verity, P. G. (1996) Micro- and mesoprotoplankton of 1408 W in the equatorial Pacific: heterotrophs and mixotrophs. Mar. Ecol. Prog. Ser., 10, 273-282.
75. Stoecker, D. K., Johnson, M. D., de Vargas, C. et al. (2009) Acquired phototrophy in aquatic protists. Aquat. Microb. Ecol., 57, 279-310.
76. Stukel, M. R., Landry, M. R. and Selph, K. E. (2011) Nanoplankton mixotrophy in the eastern equatorial Pacific. Deep-Sea Res. II, 58, 378-386.
77. Thingstad, T. F., Havskum, H., Garde, K. et al. (1996) On the strategy of "Eating your competitor": a mathematical analysis of algal mixotrophy. Ecology, 77, 2108-2118.
78. Zubkov, M. V. and Tarran, G. A. (2008) High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature, 455, 224-226.