Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences

Food chain effects of nutrient limitation in primary producers

Maarten Boersma A B F , Claes Becker C D , Arne M. Malzahn A and Sonja Vernooij C E

A Alfred Wegener Institut für Polar und Meeresforschung, Biologische Anstalt Helgoland, Postbox 180, 27483 Helgoland, Germany.

B GKSS-Research Centre, Institute for Coastal Research, Max-Planck-Straße 1, 21502 Geesthacht, Germany.

C Max Planck Institut für Limnologie, Postfach 165, 24302 Plön, Germany.

D Present address: SWECO Environment AB, Gjörwellsgatan 22, Box 34044, 10026 Stockholm, Sweden.

E Present address: Kiwa Water Research, Groningenhaven 7, 3433 PE, Nieuwegein, The Netherlands.

F Corresponding author. Email:

Marine and Freshwater Research 60(10) 983-989
Submitted: 20 August 2008  Accepted: 29 March 2009   Published: 20 October 2009


The propagation of mineral limitation in primary producers to the second consumer level has rarely been investigated. Recently, it has been shown that limitation effects do travel up the food chain, not only quantitatively, but also qualitatively, and also that these quality effects affect the nutritional condition and growth of secondary consumers. The present study experimentally investigated the effect of phosphorus limitation in combination with fatty acid addition in primary producers (Scenedesmus obliquus) channelled through a primary consumer (Daphnia magna) on the condition of larval rainbow trout (Oncorhynchus mykiss). The C : P ratio and the fatty acid concentrations of the primary producers varied significantly with the phosphorus concentration of the culture media. These differences were also visible in the primary consumers (D. magna) feeding on the algae. The significantly different stoichiometry and fatty acid concentrations of the daphnids fed to larval trout did not lead to significant differences in growth, but the additional supplementation of fatty acid emulsions caused a significant increase in the condition of the fish. It was found that in the case of Daphnia as the primary prey for fish, with its relatively high phosphorus content even under phosphorus limitation, it is unlikely that phosphorus limitation affects fish condition and growth.

Additional keywords: ecological stoichiometry, homeostasis, Redfield ratio.


Andersen T.Hessen D. O.1991Carbon, nitrogen and phosphorus content of freshwater zooplankton.Limnology and Oceanography36807814

Becker C.Boersma M.2005Differential effects of phosphorus and fatty acids on Daphnia magna growth and reproduction.Limnology and Oceanography50388397

Bell J. G.McEvoy L. A.Estevez A.Shields R. J.Sargent J. R.2003Optimising lipid nutrition in first-feeding flatfish larvae.Aquaculture227211220

Boersma M.2000The nutritional quality of P-limited algae for Daphnia.Limnology and Oceanography4511571161

Boersma M.Elser J. J.2006Too much of a good thing: on stoichiometrically balanced diets and maximal growth.Ecology8713251330

Boersma M.Stelzer C.-P.2000Response of a zooplankton community to the addition of unsaturated fatty acids: an enclosure study.Freshwater Biology45179188doi:10.1046/J.1365-2427.2000.00666.X

Boersma M.van Tongeren O. F. R.Mooij W. M.1996Seasonal patterns in the mortality of Daphnia species in a shallow lake.Canadian Journal of Fisheries and Aquatic Sciences531828doi:10.1139/CJFAS-53-1-18

Brett M. T.1993Comment on ‘Possibility of N or P limitation for planktonic cladocerans: an experimental test’ (Urabe and Watanabe) and ‘Nutrient element limitation of zooplankton production’ (Hessen).Limnology and Oceanography3813331337

Brett M. T.Müller-Navarra D. C.Ballantyne A. P.Ravet J. L.Goldman C. R.2006Daphnia fatty acid composition reflects that of their diet.Limnology and Oceanography5124282437

Bureau D. P.Hua K.Harris A. M.2008The effect of dietary lipid and long-chain n-3 PUFA levels on growth, energy utilization, carcass quality, and immune function of rainbow trout, Oncorhynchus mykiss.Journal of the World Aquaculture Society39121

Clemmesen C.1993Improvements in the fluorimetric determination of the RNA and DNA content of individual marine fish larvae.Marine Ecology Progress Series100177183doi:10.3354/MEPS100177

Coutteau P.Sorgeloos P.1997Manipulation of dietary lipids, fatty acids and vitamins in zooplankton cultures.Freshwater Biology38501512doi:10.1046/J.1365-2427.1997.00239.X

Coutteau P.Castell J. D.Ackman R. G.Sorgeloos P.1996The use of lipid emulsions as carriers for essential fatty acids in bivalves – a test case with juvenile Placopecten magellanicus.Journal of Shellfish Research15259264

DeMott W. R.Pape B. J.2005Stoichiometry in an ecological context: testing for links between Daphnia P-content, growth rate and habitat preference.Oecologia1422027

Elser J. J.Hayakawa K.Urabe J.2001Nutrient limitation reduces food quality for zooplankton: Daphnia response to seston phosphorus enrichment.Ecology82898903

Frost P. C.Ebert D.Smith V. H.2008Responses of a bacterial pathogen to phosphorus limitation of its aquatic invertebrate host.Ecology89313318

Gregory T. R.Wood C. M.1998Individual variation and interrelationships between swimming performance, growth rate, and feeding in juvenile rainbow trout (Oncorhynchus mykiss).Canadian Journal of Fisheries and Aquatic Sciences5515831590doi:10.1139/CJFAS-55-7-1583

Hessen D. O.Lyche A.1991Interspecific and intraspecific variations in zooplankton element composition.Archiv für Hydrobiologie121343353

Ho T. Y.Quigg A.Finkel Z. V.Milligan A. J.Wyman al.2003The elemental composition of some marine phytoplankton.Journal of Phycology3911451159

Jaya-Ram A.Kuah M. K.Lim P. S.Kolkovski S.Shu-Chien A. C.2008Influence of dietary HUFA levels on reproductive performance, tissue fatty acid profile and desaturase and elongase mRNAs expression in female zebrafish Danio rerio.Aquaculture277275281doi:10.1016/J.AQUACULTURE.2008.02.027

Jeppesen E.Madsen E. A.Jensen J. P.Anderson N. J.1996Reconstructing the past density of planktivorous fish and trophic structure from sedimentary zooplankton fossils – a surface sediment calibration data set from shallow lakes.Freshwater Biology36115127doi:10.1046/J.1365-2427.1996.00085.X

Klüttgen B.Dulmer U.Engels M.Ratte H. T.1994ADaM, an artificial freshwater for the culture of zooplankton.Water Research28743746doi:10.1016/0043-1354(94)90157-0

Le Pecq J. B.Paoletti C.1966A new fluorometric method for RNA and DNA determination.Analytical Biochemistry17100107doi:10.1016/0003-2697(66)90012-1

Malzahn A. M.Clemmesen C.Rosenthal H.2003Temperature effects on growth and nucleic acids in laboratory-reared larval coregonid fish.Marine Ecology Progress Series259285293doi:10.3354/MEPS259285

Malzahn A. M.Aberle N.Clemmesen C.Boersma M.2007aNutrient limitation of primary producers affects planktivorous fish condition.Limnology and Oceanography5220622071

Malzahn A. M.Clemmesen C.Wiltshire K. H.Laakmann S.Boersma M.2007bComparative nutritional condition of larval dab Limanda limanda and lesser sandeel Ammodytes marinus in a highly variable environment.Marine Ecology Progress Series334205212

Masuda R.Takeuchi T.Tsukamoto K.Sato H.Shimizu al.1999Incorporation of dietary docosahexaenoic acid into the central nervous system of the yellowtail Seriola quinqueradiata.Brain, Behavior and Evolution53173179doi:10.1159/000006592

Mourente G.Tocher D. R.1992Effects of weaning on to a pelleted diet on docosahexaenoic acid (22:6n-3) levels in the brain of developing turbot (Scophthalmus maximus L).Aquaculture105363377doi:10.1016/0044-8486(92)90100-Y

Müller-Navarra D. C.1995Biochemical versus mineral limitation in Daphnia.Limnology and Oceanography4012091214

Müller-Navarra D. C.2006The nutritional importance of polyunsaturated fatty acids and their use as trophic markers for herbivorous zooplankton: does it contradict?Archiv für Hydrobiologie167501513

Plath K.Boersma M.2001Mineral limitation of zooplankton: stoichiometric constraints and optimal foraging.Ecology8212601269

Schindler D. E.Eby L. A.1997Stoichiometry of fishes and their prey: implications for nutrient recycling.Ecology7818161831

Schoo K. L., Aberle N., Malzahn A. M., and Boersma M. (2009). Does the nutrient stoichiometry of primary producers affect the secondary consumer Pleurobrachia pileus? Aquatic Ecology, in press.

Sommer U.Sommer F.2006Cladocerans versus copepods: the cause of contrasting top–down controls on freshwater and marine phytoplankton.Oecologia147183194doi:10.1007/S00442-005-0320-0

van Densen W. L. T.1985Feeding behaviour of major 0+ fish species in a shallow, eutrophic lake (Tjeukemeer, The Netherlands).Zeitschrift für Angewandte Ichthyologie14970

Vernooij S. (2004). Effect of phosphorus limitation and fatty acid addition on Oncorhynchus mykiss larvae. M.Sc. Thesis, University of Wageningen, The Netherlands.

Vrede T.Persson J.Aronsen G.2002The influence of food quality (P : C ratio) on RNA : DNA ratio and somatic growth rate of Daphnia.Limnology and Oceanography47487494

Wilson C. M.Friesen E. N.Higgs D. A.Farrell A. P.2007The effect of dietary lipid and protein source on the swimming performance, recovery ability and oxygen consumption of Atlantic salmon (Salmo salar).Aquaculture273687699

Wiltshire K. H.Boersma M.Möller A.Buhtz H.2000Extraction of pigments and fatty acids from the green alga Scenedesmus obliquus (Chlorophyceae).Aquatic Ecology34119126doi:10.1023/A:1009911418606

Wu F. C.Ting Y. Y.Chen H. Y.2002Docosahexaenoic acid is superior to eicosapentaenoic acid as the essential fatty acid for growth of grouper, Epinephelus malabancus.The Journal of Nutrition1327279

Zehnder A. A.Gorham P. R.1960Factors influencing the growth of Microcystis aeruginosa Kütz. emend. Elenk.Canadian Journal of Microbiology6645660

Rent Article Export Citation Cited By (11)