Aquatic Ecology

, Volume 44, Issue 1, pp 233–242 | Cite as

Does the nutrient stoichiometry of primary producers affect the secondary consumer Pleurobrachia pileus?

  • Katherina L. Schoo
  • Nicole Aberle
  • Arne M. Malzahn
  • Maarten Boersma
Article

Abstract

We investigated whether phosphorus limitations of primary producers propagate upwards through the food web, not only to the primary consumer level but also onto the secondary consumers’ level. A tri-trophic food chain was used to assess the effects of phosphorus-limited phytoplankton (the cryptophyte Rhodomonas salina) on herbivorous zooplankters (the copepod Acartia tonsa) and finally on zooplanktivores (the ctenophore Pleurobrachia pileus). The algae were cultured in phosphorus-replete and phosphorus-limited media before being fed to two groups of copepods. The copepods in turn were fed to the top predator, P. pileus, in a mixture resulting in a phosphorus-gradient, ranging from copepods having received only phosphorus-replete algae to copepods reared solely on phosphorus-limited algae. The C:P ratio of the algae varied significantly between the two treatments, resulting in higher C:P ratios for those copepods feeding on phosphorus-limited algae, albeit with a significance of 0.07. The differences in the feeding environment of the copepods could be followed to Pleurobrachia pileus. Contrary to our expectations, we found that phosphorus-limited copepods represented a higher quality food source for P. pileus, as shown by the better condition (expressed as nucleic acid content) of the ctenophore. This could possibly be explained by the rather high C:P ratios of ctenophores, their resulting low phosphorus demand and relative insensitivity to P deficiency. This might potentially be an additional explanation for the observed increasing abundances of gelatinous zooplankton in our increasingly phosphorus-limited coastal seas.

Keywords

Phosphorus limitation Ctenophores Ecological stoichiometry Marine food webs Gelatinous zooplankton Trophic transfer 

References

  1. Anninsky BE, Finenko GA, Abolmasova GI, Hubareva ES, Svetlichny LS, Bat L, Kideys AE (2005) Effect of starvation on the biochemical compositions and respiration rates of ctenophores Mnemiopsis leidyi and Beroe ovata in the Black Sea. J Mar Biol Assoc UK 85:549–561CrossRefGoogle Scholar
  2. Attrill MJ, Wright J, Edwards M (2007) Climate-related increases in jellyfish frequency suggest a more gelatinous future for the North Sea. Limnol Oceanogr 52:480–485Google Scholar
  3. Boersma M, Elser JJ (2006) Too much of a good thing: on stoichiometrically balanced diets and maximal growth. Ecology 87:1325–1330CrossRefPubMedGoogle Scholar
  4. Boersma M, Kreutzer C (2002) Life at the edge: is food quality really of minor importance at low quantities? Ecology 83:2552–2561CrossRefGoogle Scholar
  5. Boersma M, Aberle N, Hantzsche FM, Schoo KL, Wiltshire KH, Malzahn AM (2008) Nutritional limitation travels up the food chain. Int Rev Hydrobiol 93:479–488CrossRefGoogle Scholar
  6. Borodkin SO, Korzhikova LI (1991) The chemical composition of the ctenophore Mnemiopsis leidyi and its role in the nutrient transformation in the Black Sea. Okeanologiya 31:754–758Google Scholar
  7. Carrillo P, Villar-Argaiz M, Medina-Sanchez JM (2001) Relationship between N:P ratio and growth rate during the life cycle of calanoid copepods: an in situ measurement. J Plankton Res 23:537–547CrossRefGoogle Scholar
  8. Clemmesen C, Buhler V, Carvalho G, Case R, Evans G, Hauser L, Hutchinson WF, Kjesbu OS, Mempel H, Moksness E, Otteraa H, Paulsen H, Thorsen A, Svaasand T (2003) Variability in condition and growth of Atlantic cod larvae and juveniles reared in mesocosms: environmental and maternal effects. J Fish Biol 62:706–723CrossRefGoogle Scholar
  9. Daly KL (2004) Overwintering growth and development of larval Euphausia superba: an interannual comparison under varying environmental conditions west of the Antarctic Peninsula. Deep-Sea Res Part II-Top Stud Oceanogr 51:2139–2168CrossRefGoogle Scholar
  10. Darchambeau F, Faerovig PJ, Hessen DO (2003) How Daphnia copes with excess carbon in its food. Oecologia 136:336–346CrossRefPubMedGoogle Scholar
  11. DeMott WR, Gulati RD, Siewertsen K (1998) Effects of phosphorus-deficient diets on the carbon and phosphorus balance of Daphnia magna. Limnol Oceanogr 43:1147–1161Google Scholar
  12. Dickmann EM, Newell JM, Gonzalez MJ, Vanni MJ (2008) Light, nutrients, and food-chain length constrain planktonic energy transfer efficiency across multiple trophic levels. Proc Natl Acad Sci USA 105:18408–18412CrossRefGoogle Scholar
  13. Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley E, Schulz KL, Siemann EH, Sterner RW (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580CrossRefPubMedGoogle Scholar
  14. Elser JJ, Hayakawa K, Urabe J (2001) Nutrient limitation reduces food quality for zooplankton: Daphnia response to seston phosphorus enrichment. Ecology 82:898–903Google Scholar
  15. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142CrossRefPubMedGoogle Scholar
  16. Ferron A, Leggett WC (1994) An appraisal of condition measures for marine fish larvae. Adv Mar Biol 30:217–303CrossRefGoogle Scholar
  17. Fraser JH (1970) The ecology of the ctenophore Pleurobrachia pileus in scottish waters. ICES J Mar Res 33:149–168CrossRefGoogle Scholar
  18. Frost PC, Ebert D, Smith VH (2008) Responses of a bacterial pathogen to phosphorus limitation of its aquatic invertebrate host. Ecology 89:313–318CrossRefPubMedGoogle Scholar
  19. Gaedke U, Hochstadter S, Straile D (2002) Interplay between energy limitation and nutritional deficiency: empirical data and food web models. Ecol Monogr 72:251–270CrossRefGoogle Scholar
  20. Gibbons MJ, Painting SJ (1992) The effects and implications of container volume on clearance rates of the ambush entangling predator Pleurobrachia pileus (Ctenophora: Tentaculata). J Exp Mar Biol Ecol 163:199–208CrossRefGoogle Scholar
  21. Gorokhova E (2003) Relationships between nucleic acid levels and egg production rates in Acartia bifilosa: implications for growth assessment of copepods in situ. Mar Ecol Prog Ser 262:163–172CrossRefGoogle Scholar
  22. Grasshoff K, Kremling K, Ehrhardt M (1999) Methods of seawater analysis. Wiley, New YorkCrossRefGoogle Scholar
  23. Greve W (1970) Cultivation experiments on North Sea ctenophores. Helgol Wiss Meeresunters 20:304–317CrossRefGoogle Scholar
  24. Greve W (1972) Ökologische Untersuchungen an Pleurobrachia pileus 2. Laboruntersuchungen. Helgol Wiss Meeresunters 23:141–164CrossRefGoogle Scholar
  25. Greve W, Reiners F, Nast J, Hoffmann S (2004) Helgoland Roads meso- and macrozooplankton time-series 1974 to 2004: lessons from 30 years of single spot, high frequency sampling at the only off-shore island of the North Sea. Helgol Mar Res 58:274–288CrossRefGoogle Scholar
  26. Guillard RR, Ryther J (1962) Studies of marine planktonic diatoms. Can J Microbiol 8:229–239CrossRefPubMedGoogle Scholar
  27. Hamer H (2008) On the feeding ecology of ctenophores in the German Bight. Diploma thesis, University of KielGoogle Scholar
  28. IPCC (2007) Intergovernmental panel on climate change: climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  29. Kremer P (1977) Respiration and excretion by ctenophore Mnemiopsis leidyi. Mar Biol 44:43–50CrossRefGoogle Scholar
  30. Kremer P (1982) Effect of food availability on the metabolism of the ctenophore Mnemiopsis mccradyi. Mar Biol 71:149–156CrossRefGoogle Scholar
  31. Kremer P, Canino MF, Gilmer RW (1986) Metabolism of epipelagic tropical ctenophores. Mar Biol 90:403–412CrossRefGoogle Scholar
  32. Le Pecq JB, Paoletti C (1966) A new fluorometric method for RNA and DNA determination. Anal Biochem 17:100–107CrossRefPubMedGoogle Scholar
  33. Malzahn AM, Aberle N, Clemmesen C, Boersma M (2007a) Nutrient limitation of primary producers affects planktivorous fish condition. Limnol Oceanogr 52:2062–2071Google Scholar
  34. Malzahn AM, Clemmesen C, Wiltshire KH, Laakmann S, Boersma M (2007b) Comparative nutritional condition of larval dab Limanda limanda and lesser sandeel Ammodytes marinus in a highly variable environment. Mar Ecol Prog Ser 334:205–212CrossRefGoogle Scholar
  35. Melzner F, Forsythe JW, Lee PG, Wood JB, Piatkowski U, Clemmesen C (2005) Estimating recent growth in the cuttlefish Sepia officinalis: are nucleic acid-based indicators for growth and condition the method of choice? J Exp Mar Biol Ecol 317:37–51CrossRefGoogle Scholar
  36. Parslow-Williams P, Atkinson RJA, Taylor AC (2001) Nucleic acids as indicators of nutritional condition in the Norway lobster Nephrops norvegicus. Mar Ecol Prog Ser 211:235–243CrossRefGoogle Scholar
  37. Plath K, Boersma M (2001) Mineral limitation of zooplankton: stoichiometric constraints and optimal foraging. Ecology 82:1260–1269CrossRefGoogle Scholar
  38. Reeve MR, Walter MA, Ikeda T (1978) Laboratory studies of ingestion and food utilization in lobate and tentaculate ctenophores. Limnol Oceanogr 23:740–751Google Scholar
  39. Schneider G (1989) Zur chemischen Zusammensetzung der Ctenophore Pleurobrachia pileus in der Kieler Bucht. Helgol Wiss Meeresunters 43:67–76CrossRefGoogle Scholar
  40. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, PrincetonGoogle Scholar
  41. Sterner RW, George NB (2000) Carbon, nitrogen, and phosphorus stoichiometry of cyprinid fishes. Ecology 81:127–140CrossRefGoogle Scholar
  42. Sterner RW, Hessen DO (1994) Algal nutrient limitation and the nutrition of aquatic herbivores. Annu Rev Ecol Syst 25:1–29CrossRefGoogle Scholar
  43. Sterner RW, Clasen J, Lampert W, Weisse T (1998) Carbon: phosphorus stoichiometry and food chain production. Ecol Lett 1:146–150CrossRefGoogle Scholar
  44. Urabe J, Clasen J, Sterner RW (1997) Phosphorus limitation of Daphnia growth: is it real? Limnol Oceanogr 42:1436–1443CrossRefGoogle Scholar
  45. Urabe J, Togari J, Elser JJ (2003) Stoichiometric impacts of increased carbon dioxide on a planktonic herbivore. Glob Chang Biol 9:818–825CrossRefGoogle Scholar
  46. van der Zee C, Chou L (2005) Seasonal cycling of phosphorus in the Southern Bight of the North Sea. Biogeosciences 2:27–42CrossRefGoogle Scholar
  47. Van Nieuwerburgh L, Wanstrand I, Snoeijs P (2004) Growth and C:N:P ratios in copepods grazing on N- or Si-limited phytoplankton blooms. Hydrobiologia 514:57–72CrossRefGoogle Scholar
  48. Vermaat JE, McQuatters-Gollop A, Eleveld MA, Gilbert AJ (2008) Past, present and future nutrient loads of the North Sea: causes and consequences. Estuar Coast Shelf Sci 80:53–59CrossRefGoogle Scholar
  49. Villar-Argaiz M, Medina-Sanchez JM, Carrillo P (2002) Linking life history strategies and ontogeny in crustacean zooplankton: implications for homeostasis. Ecology 83:1899–1914CrossRefGoogle Scholar
  50. White TCR (1993) The inadequate environment. Springer, BerlinGoogle Scholar
  51. Wiltshire KH, Malzahn AM, Kai Wirtz K, Greve W, Janisch S, Mangelsdorf P, Manly BFJ, Boersma M (2008) Resilience of North Sea phytoplankton spring blooms dynamics: an analysis of long term data at Helgoland Roads. Limnol Oceanogr 53:1294–1302Google Scholar
  52. Youngbluth MJ, Kremer P, Bailey TG, Jacoby CA (1988) Chemical-composition, metabolic rates and feeding-behavior of the midwater ctenophore Bathocyroe fosteri. Mar Biol 98:87–94CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Katherina L. Schoo
    • 1
    • 2
  • Nicole Aberle
    • 1
  • Arne M. Malzahn
    • 1
  • Maarten Boersma
    • 1
    • 3
  1. 1.Alfred-Wegener-Institut für Polar- und MeeresforschungBiologische Anstalt HelgolandHelgolandGermany
  2. 2.Leibniz Institute of Marine SciencesIFM-GeomarKielGermany
  3. 3.GKSS-Research CentreInstitute for Coastal ResearchGeesthachtGermany

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