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

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
+ Author Affiliations
- Author Affiliations

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: maarten.boersma@awi.de

Marine and Freshwater Research 60(10) 983-989 https://doi.org/10.1071/MF08240
Submitted: 20 August 2008  Accepted: 29 March 2009   Published: 20 October 2009

Abstract

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.


Acknowledgements

We thank Winfried Lampert for his hospitability at the Max Planck Institute, and for helpful discussions. Martin Kalbe, Dieter Albrecht, Gerhard Augustin, Heike Wardenga, Maren Volquardsen and Heinke Buhtz are thanked for their help with different aspects of the experiments from keeping fish alive to culturing algae as food for zooplankters. We thank Albrecht Hahn from the Fischbrutanstalt Altmühlendorf for the supply of the egg incubation devices and for helpful practical tips on rearing trout, and two anonymous reviewers for their many helpful comments. This study complies with current German law on animal studies.


References

Andersen, T. , and Hessen, D. O. (1991). Carbon, nitrogen and phosphorus content of freshwater zooplankton. Limnology and Oceanography 36, 807–814.
CAS | CAS |

Becker, C. , and Boersma, M. (2005). Differential effects of phosphorus and fatty acids on Daphnia magna growth and reproduction. Limnology and Oceanography 50, 388–397.
CAS |

Bell, J. G. , McEvoy, L. A. , Estevez, A. , Shields, R. J. , and Sargent, J. R. (2003). Optimising lipid nutrition in first-feeding flatfish larvae. Aquaculture 227, 211–220.
CrossRef | CAS | CAS |

Boersma, M. (2000). The nutritional quality of P-limited algae for Daphnia. Limnology and Oceanography 45, 1157–1161.
CAS | CAS |

Boersma, M. , and Elser, J. J. (2006). Too much of a good thing: on stoichiometrically balanced diets and maximal growth. Ecology 87, 1325–1330.
CrossRef | PubMed | PubMed |

Boersma, M. , and Stelzer, C.-P. (2000). Response of a zooplankton community to the addition of unsaturated fatty acids: an enclosure study. Freshwater Biology 45, 179–188.
CrossRef | CAS | CAS |

Boersma, M. , van Tongeren, O. F. R. , and Mooij, W. M. (1996). Seasonal patterns in the mortality of Daphnia species in a shallow lake. Canadian Journal of Fisheries and Aquatic Sciences 53, 18–28.
CrossRef |

Brett, M. T. (1993). Comment 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 Oceanography 38, 1333–1337.
CAS | CAS |

Brett, M. T. , Müller-Navarra, D. C. , Ballantyne, A. P. , Ravet, J. L. , and Goldman, C. R. (2006). Daphnia fatty acid composition reflects that of their diet. Limnology and Oceanography 51, 2428–2437.
CAS | CAS |

Bureau, D. P. , Hua, K. , and Harris, A. M. (2008). The 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 Society 39, 1–21.
CrossRef |

Clemmesen, C. (1993). Improvements in the fluorimetric determination of the RNA and DNA content of individual marine fish larvae. Marine Ecology Progress Series 100, 177–183.
CrossRef | CAS | CAS |

Coutteau, P. , and Sorgeloos, P. (1997). Manipulation of dietary lipids, fatty acids and vitamins in zooplankton cultures. Freshwater Biology 38, 501–512.
CrossRef | CAS | CAS |

Coutteau, P. , Castell, J. D. , Ackman, R. G. , and Sorgeloos, P. (1996). The use of lipid emulsions as carriers for essential fatty acids in bivalves – a test case with juvenile Placopecten magellanicus. Journal of Shellfish Research 15, 259–264.


DeMott, W. R. , and Pape, B. J. (2005). Stoichiometry in an ecological context: testing for links between Daphnia P-content, growth rate and habitat preference. Oecologia 142, 20–27.
CrossRef | PubMed | PubMed |

Elser, J. J. , Hayakawa, K. , and Urabe, J. (2001). Nutrient limitation reduces food quality for zooplankton: Daphnia response to seston phosphorus enrichment. Ecology 82, 898–903.


Frost, P. C. , Ebert, D. , and Smith, V. H. (2008). Responses of a bacterial pathogen to phosphorus limitation of its aquatic invertebrate host. Ecology 89, 313–318.
CrossRef | PubMed | PubMed |

Gregory, T. R. , and Wood, C. M. (1998). Individual variation and interrelationships between swimming performance, growth rate, and feeding in juvenile rainbow trout (Oncorhynchus mykiss). Canadian Journal of Fisheries and Aquatic Sciences 55, 1583–1590.
CrossRef |

Hessen, D. O. , and Lyche, A. (1991). Interspecific and intraspecific variations in zooplankton element composition. Archiv für Hydrobiologie 121, 343–353.


Ho, T. Y. , Quigg, A. , Finkel, Z. V. , Milligan, A. J. , and Wyman, K. , et al. (2003). The elemental composition of some marine phytoplankton. Journal of Phycology 39, 1145–1159.
CrossRef | CAS | CAS |

Jaya-Ram, A. , Kuah, M. K. , Lim, P. S. , Kolkovski, S. , and Shu-Chien, A. C. (2008). Influence of dietary HUFA levels on reproductive performance, tissue fatty acid profile and desaturase and elongase mRNAs expression in female zebrafish Danio rerio. Aquaculture 277, 275–281.
CrossRef | CAS | CAS |

Jeppesen, E. , Madsen, E. A. , Jensen, J. P. , and Anderson, N. J. (1996). Reconstructing the past density of planktivorous fish and trophic structure from sedimentary zooplankton fossils – a surface sediment calibration data set from shallow lakes. Freshwater Biology 36, 115–127.
CrossRef |

Klüttgen, B. , Dulmer, U. , Engels, M. , and Ratte, H. T. (1994). ADaM, an artificial freshwater for the culture of zooplankton. Water Research 28, 743–746.
CrossRef |

Le Pecq, J. B. , and Paoletti, C. (1966). A new fluorometric method for RNA and DNA determination. Analytical Biochemistry 17, 100–107.
CrossRef | CAS | CAS | PubMed | PubMed |

Malzahn, A. M. , Clemmesen, C. , and Rosenthal, H. (2003). Temperature effects on growth and nucleic acids in laboratory-reared larval coregonid fish. Marine Ecology Progress Series 259, 285–293.
CrossRef | CAS | CAS |

Malzahn, A. M. , Aberle, N. , Clemmesen, C. , and Boersma, M. (2007a). Nutrient limitation of primary producers affects planktivorous fish condition. Limnology and Oceanography 52, 2062–2071.
CAS | CAS |

Malzahn, A. M. , Clemmesen, C. , Wiltshire, K. H. , Laakmann, S. , and Boersma, M. (2007b). Comparative nutritional condition of larval dab Limanda limanda and lesser sandeel Ammodytes marinus in a highly variable environment. Marine Ecology Progress Series 334, 205–212.
CrossRef | CAS | CAS |

Masuda, R. , Takeuchi, T. , Tsukamoto, K. , Sato, H. , and Shimizu, K. , et al. (1999). Incorporation of dietary docosahexaenoic acid into the central nervous system of the yellowtail Seriola quinqueradiata. Brain, Behavior and Evolution 53, 173–179.
CrossRef | CAS | CAS | PubMed | PubMed |

Mourente, G. , and Tocher, D. R. (1992). Effects of weaning on to a pelleted diet on docosahexaenoic acid (22:6n-3) levels in the brain of developing turbot (Scophthalmus maximus L). Aquaculture 105, 363–377.
CrossRef | CAS | CAS |

Müller-Navarra, D. C. (1995). Biochemical versus mineral limitation in Daphnia. Limnology and Oceanography 40, 1209–1214.


Müller-Navarra, D. C. (2006). The nutritional importance of polyunsaturated fatty acids and their use as trophic markers for herbivorous zooplankton: does it contradict? Archiv für Hydrobiologie 167, 501–513.
CrossRef |

Plath, K. , and Boersma, M. (2001). Mineral limitation of zooplankton: stoichiometric constraints and optimal foraging. Ecology 82, 1260–1269.


Schindler, D. E. , and Eby, L. A. (1997). Stoichiometry of fishes and their prey: implications for nutrient recycling. Ecology 78, 1816–1831.


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. doi:10.1007/S10452-009-9265-4

Sommer, U. , and Sommer, F. (2006). Cladocerans versus copepods: the cause of contrasting top–down controls on freshwater and marine phytoplankton. Oecologia 147, 183–194.
CrossRef | PubMed | PubMed |

van Densen, W. L. T. (1985). Feeding behaviour of major 0+ fish species in a shallow, eutrophic lake (Tjeukemeer, The Netherlands). Zeitschrift für Angewandte Ichthyologie 1, 49–70.


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. , and Aronsen, G. (2002). The influence of food quality (P : C ratio) on RNA : DNA ratio and somatic growth rate of Daphnia. Limnology and Oceanography 47, 487–494.
CAS | CAS |

Wilson, C. M. , Friesen, E. N. , Higgs, D. A. , and Farrell, A. P. (2007). The effect of dietary lipid and protein source on the swimming performance, recovery ability and oxygen consumption of Atlantic salmon (Salmo salar). Aquaculture 273, 687–699.
CrossRef | CAS | CAS |

Wiltshire, K. H. , Boersma, M. , Möller, A. , and Buhtz, H. (2000). Extraction of pigments and fatty acids from the green alga Scenedesmus obliquus (Chlorophyceae). Aquatic Ecology 34, 119–126.
CrossRef | CAS | CAS |

Wu, F. C. , Ting, Y. Y. , and Chen, H. Y. (2002). Docosahexaenoic acid is superior to eicosapentaenoic acid as the essential fatty acid for growth of grouper, Epinephelus malabancus. The Journal of Nutrition 132, 72–79.
CAS | CAS | PubMed | PubMed |

Zehnder, A. A. , and Gorham, P. R. (1960). Factors influencing the growth of Microcystis aeruginosa Kütz. emend. Elenk. Canadian Journal of Microbiology 6, 645–660.
CAS | CAS | PubMed | PubMed |



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