Zooplankton-mediated nutrient limitation patterns in marine phytoplankton: An experimental approach with natural communities

Marine Ecology Progress Series

Volumn 449, Issue , 2012, Pages 83-94

  Trommer, Gabriele ^a   Pondaven, Philippe ^a   Siccha, Michael ^b   Stibor, Herwig ^a  

^a Universite de Bretagne Occidentale   (France)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Marine plankton; Nutrient limitation; Stoichiometry; Zooplankton driven nutrient recycling

Indexed keywords

AQUATIC ORGANISM; BIOASSAY; COMMUNITY STRUCTURE; EXPERIMENTAL STUDY; GRAZING; MARINE ENVIRONMENT; NITROGEN; NUTRIENT CYCLING; NUTRIENT LIMITATION; PHOSPHORUS; PHYTOPLANKTON; POPULATION DENSITY; STOCHASTICITY; ZOOPLANKTON;

COPEPODA; ROTIFERA;

EID: 84858124883     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps09508     Document Type: Article

References (78)

1. Allan JD (1976) Life-history patterns in zooplankton. Am Nat 110: 165-180
2. Andersen T, Hessen DO (1991) Carbon, nitrogen, and phosphorus-content of fresh-water zooplankton. Limnol Ocea nogr 36: 807-814 (Pubitemid 23395407)
3. Beman JM, Arrigo KR, Matson PA (2005) Agricultural runoff fuels large phytoplankton blooms in vulnerable areas of the ocean. Nature 434: 211-214 (Pubitemid 40388050)
4. Boyd PW, Watson AJ, Law CS, Abraham ER and others (2000) A mesoscale phytoplankton bloom in the polar southern ocean stimulated by iron fertilization. Nature 407: 695-702
5. Brzezinski MA, Baines SB, Balch WM, Beucher CP and others (2011) Co-limitation of diatoms by iron and silicic acid in the equatorial pacific. Deep-Sea Res II 58: 493-511
6. Chen M, Liu H (2011) Experimental simulation of trophic interactions among omnivorous copepods, heterotrophic dinoflagellates and diatoms. J Exp Mar Biol Ecol 403: 65-74
7. Cherif M, Loreau M (2009) When microbes and consumers determine the limiting nutrient of autotrophs: a theoretical analysis. Proc Biol Sci 276: 487-497
8. Coale KH, Johnson KS, Fitzwater SE, Gordon RM and others (1996) A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the equa torial Pacific Ocean. Nature 383: 495-501 (Pubitemid 27040525)
9. Copin-Montegut C, Copin-Montegut G (1983) Stoichiometry of carbon, nitrogen, and phosphorus in marine particulate matter. Deep-Sea Res I 30: 31-46 (Pubitemid 13524152)
10. Corner EDS, Davies AG (1971) Plankton as a factor in nitrogen and phosphorus cycles in sea. Adv Mar Biol 9: 101-204
11. Czamanski M, Nugraha A, Pondaven P, Lasbleiz M and others (2011) Carbon, nitrogen and phosphorus elemental stoichiometry in aquacultured and wild-caught fish and consequences for pelagic nutrient dynamics. Mar Biol 158:2847-2862
12. Danger M, Oumarou C, Benest D, Lacroix G (2007) Bacteria can control stoichiometry and nutrient limitation of phyto plankton. Funct Ecol 21: 202-210 (Pubitemid 46426586)
13. Del Amo Y, Le Pape O, Treguer P, Queguiner B, Menesguen A, Aminot A (1997) Impacts of high-nitrate freshwater inputs on macrotidal ecosystems. I. Seasonal evolution of nutrient limitation for the diatom-dominated phytoplankton of the Bay of Brest (France). Mar Ecol Prog Ser 161: 213-224 (Pubitemid 28094355)
14. Delmas R, Hafsaoui M, Le Jehan S, Quéguiner B, Tréguer P (1983) Impact de fertilisations à forte variabilité saisonnière et annuelle sur le phytoplancton d'un écosystè me eutrophe. Oceanologica Acta Actes 17e Symposium Européen de Biologie Marine, Brest, p 81-85
15. Diehl S (2002) Phytoplankton, light, and nutrients in a gradient of mixing depths: theory. Ecology 83: 386-398 (Pubitemid 34122452)
16. Elser JJ, Hassett RP (1994) A stoichiometric analysis of the zooplankton-phytoplankton interaction in marine and freshwater ecosystems. Nature 370: 211-213
17. Elser JJ, Urabe J (1999) The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80: 735-751 (Pubitemid 29188314)
18. Elser JJ, Elser MM, Mackay NA, Carpenter SR (1988) Zooplankton- mediated transitions between N-limited and Plimited algal growth. Limnol Oceanogr 33: 1-14
19. Elser J, Marzolf E, Goldman C (1990) Phosphorus and nitrogen limitation of phytoplankton growth in the freshwaters of North America: a review and critique of experimental enrichments. Can J Fish Aquat Sci 47: 1468-1477. doi: 10.1139/f90-165
20. Elser JJ, Bracken MES, Cleland EE, Gruner DS and others (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10: 1135-1142 (Pubitemid 350060402)
21. Fisher TR, Peele ER, Ammerman JW, Harding LW (1992) Nutrient limitation of phytoplankton in Chesapeake Bay. Mar Ecol Prog Ser 82: 51-63
22. Fowler SW (1977) Trace-elements in zooplankton particulate products. Nature 269: 51-53
23. Gaudy R, Youssara F, Diaz F, Raimbault P (2003) Biomass, metabolism and nutrition of zooplankton in the Gulf of Lions (NW Mediterranean). Oceanol Acta 26: 357-372 (Pubitemid 37216141)
24. Geider RJ, La Roche J (2002) Redfield revisited: variability of C: N: P in marine microalgae and its biochemical basis. Eur J Phycol 37: 1-17 (Pubitemid 34264641)
25. Gilbert JJ, Jack JD (1993) Rotifers as predators on small ciliates. Hydrobiologia 255-256: 247-253 (Pubitemid 24412589)
26. Gismervik I (1997) Stoichiometry of some marine planktonic crustaceans. J Plankton Res 19: 279-285 (Pubitemid 27347717)
27. Goldman JC, McCarthy JJ, Peavey DG (1979) Growth-rate influence on the chemical composition of phytoplankton in oceanic waters. Nature 279: 210-215
28. Guildford SJ, Hecky RE (2000) Total nitrogen, total phosphorus, and nutrient limitation in lakes and oceans: is there a common relationship? Limnol Oceanogr 45: 1213-1223
29. Hannides CCS, Landry MR, Benitez-Nelson CR, Styles RM, Montoya JP, Karl DM (2009) Export stoichiometry and migrant-mediated flux of phosphorus in the North Pacific Subtropical Gyre. Deep-Sea Res I 56: 73-88
30. Harpole WS, Ngai JT, Cleland EE, Seabloom EW and others (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14: 852-862
31. Hassett RP, Cardinale B, Stabler LB, Elser JJ (1997) Ecological stoichiometry of N and P in pelagic ecosystems: comparison of lakes and oceans with emphasis on the zooplankton-phytoplankton interaction. Limnol Oceanogr 42: 648-662 (Pubitemid 27468389)
32. Healey FP (1985) Interacting effects of light and nutrient limitation on the growth-rate of Synechococcus linearis (Cyanophyceae). J Phycol 21: 134-146
33. Hecky RE, Kilham P (1988) Nutrient limitation of phytoplankton in freshwater and marine environments: A review of recent evidence on the effects of enrichment. Limnol Oceanogr 33: 796-822
34. Hecky RE, Campbell P, Hendzel LL (1993) The stoichiometry of carbon, nitrogen, and phosphorus in particulate matter of lakes and oceans. Limnol Oceanogr 38: 709-724 (Pubitemid 24393434)
35. Hessen DO, Agren GI, Anderson TR, Elser JJ, De Ruiter PC (2004) Carbon sequestration in ecosystems: the role of stoichiometry. Ecology 85: 1179-1192 (Pubitemid 39188075)
36. Hjerne O, Hansson S (2002) The role of fish and fisheries in Baltic Sea nutrient dynamics. Limnol Oceanogr 47: 1023-1032 (Pubitemid 34793736)
37. Hutchins DA, Bruland KW (1998) Iron-limited diatom growth and Si: N uptake ratios in a coastal upwelling regime. Nature 393: 561-564 (Pubitemid 28319241)
38. Karl DM (1999) A sea of change: Biogeochemical variability in the North Pacific Subtropical Gyre. Ecosystems (N Y) 2: 181-214 (Pubitemid 29332242)
39. Karl DM, Bjorkman KM, Dore JE, Fujieki L and others (2001a) Ecological nitrogen-to-phosphorus at station ALOHA. Deep-Sea Res Part II 48: 1529-1566
40. Karl DM, Bidigare RR, Letelier RM (2001b) Long-term changes in plankton community structure and produc - tivity in the North Pacific Subtropical Gyre: The domain shift hypothesis. Deep-Sea Res II 48: 1449-1470 (Pubitemid 32434563)
41. Klausmeier CA, Litchman E, Levin SA (2004a) Phytoplankton growth and stoichiometry under multiple nutrient limitation. Limnol Oceanogr 49: 1463-1470 (Pubitemid 39040326)
42. Klausmeier CA, Litchman E, Daufresne T, Levin SA (2004b) Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature 429: 171-174 (Pubitemid 38656190)
43. Koutsikopoulos C, LeCann B (1996) Physical processes and hydrological structures related to the Bay of Biscay anchovy. Sci Mar 60: 9-19 (Pubitemid 126653286)
44. Laes A, Vuillemin R, Leilde B, Sarthou G, Bournot-Marec C, Blain S (2005) Impact of environmental factors on in situ determination of iron in seawater by flow injection analysis. Mar Chem 97: 347-356 (Pubitemid 41572655)
45. Lagus A, Suomela J, Weithoff G, Heikkila K, Helminen H, Sipura J (2004) Species-specific differences in phytoplankton responses to N and P enrichments and the N: P ratio in the Archipelago Sea, northern Baltic Sea. J Plankton Res 26: 779-798 (Pubitemid 38940838)
46. LeBorgne R (1982) Zooplankton production in the eastern tropical Atlantic Ocean: Net growth efficiency and P: B in terms of carbon, nitrogen, and phosphorus. Limnol Oceanogr 27: 681-698
47. Main TM, Dobberfuhl DR, Elser JJ (1997) N: P stoichiometry and ontogeny of crustacean zooplankton: A test of the growth rate hypothesis. Limnol Oceanogr 42: 1474-1478 (Pubitemid 28290208)
48. Masuzawa T, Koyama M, Terazaki M (1988) A regularity in trace-element contents of marine zooplankton species. Mar Biol 97: 587-591
49. Moutin T, Van Den Broeck N, Beker B, Dupouy C, Rimmelin P, Le Bouteiller A (2005) Phosphate availability controls Trichodesmium spp. biomass in the SW Pacific Ocean. Mar Ecol Prog Ser 297: 15-21 (Pubitemid 41215411)
50. Nugraha A, Pondaven P, Treguer P (2010) Influence of consumer-driven nutrient recycling on primary production and the distribution of N and P in the ocean. Biogeosciences 7: 1285-1305
51. Polovina JJ, Howell EA, Abecassis M (2008) Ocean's least productive waters are expanding. Geophys Res Lett 35: L03618. doi: 10.1029/2007/GL031745
52. Quigg A, Finkel ZV, Irwin AJ, Rosenthal Y and others (2003) The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature 425: 291-294 (Pubitemid 37158404)
53. Redfield AC (1958) The biological control of chemical factors in the environment. Am Sci 46: 205-221
54. Rhee G, Gotham I (1980) Optimum N: P ratios and coexistence of planktonic algae. J Phycol 16: 486-489
55. Rothhaupt KO (1995) Algal nutrient limitation affects rotifer growth rate but not ingestion rate. Limnol Oceanogr 40: 1201-1208 (Pubitemid 3016464)
56. Ryther JH, Dunstan WM (1971) Nitrogen, phosphorus, and eutrophication in coastal marine environments. Science 171: 1008-1013
57. Sañudo-Wilhelmy SA, Kustka AB, Gobler CJ, Hutchins DA and others (2001) Phosphorus limitation of nitrogen fixation by Trichodesmium in the central Atlantic Ocean. Nature 411: 66-69 (Pubitemid 32428189)
58. Sarthou G, Vincent D, Christaki U, Obernosterer I, Timmermans KR, Brussaard CPD (2008) The fate of biogenic iron during a phytoplankton bloom induced by natural fertilisation: Impact of copepod grazing. Deep-Sea Res II 55: 734-751
59. Schindler DW (1977) Evolution of phosphorus limitation in lakes. Science 195: 260-262
60. Sommer F (2003) A comparison of the impact of major mesozooplankton taxa on marine, brackish and freshwater phyto plankton during summer. PhD thesis, Christian-Albrechts-Universität Kiel
61. Sommer U, Sommer F, Santer B, Jamieson C, Boersma M, Becker C, Hansen T (2001) Complementary impact of copepods and cladocerans on phytoplankton. Ecol Lett 4: 545-550 (Pubitemid 33105367)
62. Sommer U, Sommer F, Feuchtmayr H, Hansen T (2004) The influence of mesozooplankton on phytoplankton nutrient limitation: A mesocosm study with northeast Atlantic plankton. Protist 155: 295-304 (Pubitemid 39384651)
63. Steinberg DK, Goldthwait SA, Hansell DA (2002) Zooplankton vertical migration and the active transport of dissolved organic and inorganic nitrogen in the Sargasso Sea. Deep-Sea Res I 49: 1445-1461 (Pubitemid 34973574)
64. Stemberger RS, Miller EK (1998) A zooplankton-N: P-ratio indicator for lakes. Environ Monit Assess 51: 29-51
65. Sterner RW (1990) The ratio of nitrogen to phosphorus resupplied by herbivores: zooplankton and the algal competitive arena. Am Nat 136: 209-229
66. Sterner RW, Hessen DO (1994) Algal nutrient limitation and the nutrition of aquatic herbivores. Annu Rev Ecol Syst 25: 1-29 (Pubitemid 24986110)
67. Sterner RW, Elser JJ, Hessen DO (1992) Stoichiometric relationships among producers, consumers and nutrient cycling in pelagic ecosystems. Biogeochemistry 17: 49-67 (Pubitemid 23397428)
68. Sterner RW, Elser JJ, Fee EJ, Guildford SJ, Chrzanowski TH (1997) The light: nutrient ratio in lakes: The balance of energy and materials affects ecosystem structure and process. Am Nat 150: 663-684 (Pubitemid 27510432)
69. Sterner RW, Andersen T, Elser JJ, Hessen DO, Hood JM, McCauley E, Urabe J (2008) Scale-dependent carbon: nitrogen: phosphorus seston stoichiometry in marine and freshwaters. Limnol Oceanogr 53: 1169-1180 (Pubitemid 351821710)
70. Tamminen T, Andersen T (2007) Seasonal phytoplankton nutrient limitation patterns as revealed by bioassays over Baltic Sea gradients of salinity and eutrophication. Mar Ecol Prog Ser 340: 121-138 (Pubitemid 47122015)
71. Touratier F, Field JG, Moloney CL (2001) A stoichiometric model relating growth substrate quality (C: N: P ratios) to N: P ratios in the products of heterotrophic release and excretion. Ecol Modell 139: 265-291 (Pubitemid 32515787)
72. Tyrrell T (1999) The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400: 525-531 (Pubitemid 29381794)
73. Urabe J (1993) N-cycling and P-cycling coupled by grazers' activities: Food quality and nutrient release by zooplankton. Ecology 74: 2337-2350
74. Walve J, Larsson U (1999) Carbon, nitrogen and phosphorus stoichiometry of crustacean zooplankton in the Baltic Sea: Implications for nutrient recycling. J Plankton Res 21: 2309-2321 (Pubitemid 30018153)
75. Wang WX (2002) Interactions of trace metals and different marine food chains. Mar Ecol Prog Ser 243: 295-309
76. Wang WX, Dei RCH (2001) Biological uptake and assimilation of iron by marine plankton: influences of macronutrients. Mar Chem 74: 213-226 (Pubitemid 32258390)
77. Weber TS, Deutsch C (2010) Ocean nutrient ratios governed by plankton biogeography. Nature 467: 550-554
78. Wu J, Sunda W, Boyle EA, Karl DM (2000) Phosphate depletion in the western North Atlantic Ocean. Science 289: 759-762 (Pubitemid 30650192)