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Dietary-induced responses in the phagotrophic flagellate Oxyrrhis marina

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Abstract

Primary producers may be limited by different nutrients as well as by light availability, which in turn affects their quality as food for higher trophic levels. Typically, algae with high C:N and/or C:P ratios are low-quality food for consumers. Heterotrophic protists are important grazers on these autotrophes, but despite their importance as grazers, knowledge of food quality effects on heterotrophic protists is sparse. In the present study, we examined how differently grown Rhodomonas salina (nutrient replete, N-limited and P-limited) affected the phagotrophic flagellate Oxyrrhis marina. The functional response of O. marina (based on ingested biovolume) did not show significant differences between food sources, thus food uptake was independent of food quality. O. marina was weakly homoeostatic which means that its C:N:P ratio still reflected the elemental composition of its food to some extent. Food quality had a significantly negative effect on the numerical response of O. marina. Whereas N-limited R. salina and nutrient replete R. salina resulted in similar growth rates, P-limited algae had a significantly negative effect on the specific growth rate of O. marina. Hence, the lack of elemental phosphorus of O. marina feeding on P-limited algae caused a reduction in growth. Thus, despite their weaker homoeostasis, heterotrophic protists are also affected by high C:P food in a similar way to crustacean zooplankton.

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References

  • Aberle N, Malzahn AM (2007) Interspecific and nutrient-dependent variations in stable isotope fractionation: experimental studies simulating pelagic multitrophic systems. Oecologia 154:291–303

    Article  CAS  Google Scholar 

  • Anderson TR, Hessen DO, Elser JJ, Urabe J (2005) Metabolic stoichiometry and the fate of excess carbon and nutrients in consumers. Am Nat 165:1–15

    Article  Google Scholar 

  • Augustin CB, Boersma M (2006) Effects of nitrogen stressed algae on different Acartia species. J Plankton Res 28:429–436

    Article  Google Scholar 

  • Barlow RG, Burkill PH, Mantoura RFC (1988) Grazing and degradation of algal pigments by marine protozoan Oxyrrhis marina. J Exp Mar Biol Ecol 119:119–129

    Article  CAS  Google Scholar 

  • Boersma M, Kreutzer C (2002) Life at the edge: is food quality really of minor importance at low quantities? Ecology 83:2552–2561

    Article  Google Scholar 

  • Burns CW (1995) Effects of crowding and different food levels on growth and reproductive investment of Daphnia. Oecologia 101:234–244

    Article  Google Scholar 

  • Burns CW (2000) Crowding-induced changes in growth, reproduction and morphology of Daphnia. Freshw Biol 43:19–29

    Article  Google Scholar 

  • Clark LL, Ingall ED, Benner R (1998) Marine phosphorus is selectively remineralized. Nature 393:426–436

    Article  CAS  Google Scholar 

  • Darchambeau F, Faerovig PJ, Hessen DO (2003) How Daphnia copes with excess carbon in its food. Oecologia 136:336–346

    Article  Google Scholar 

  • Davidson K, Roberts EC, Wilson AM, Mitchell E (2005) The role of prey nutritional status in governing protozoan nitrogen regeneration efficiency. Protist 156:45–62

    Article  CAS  Google Scholar 

  • DeMott WR, Gulati RD, Van Donk E (2001) Effects of dietary phosphorus deficiency on the abundance, phosphorus balance, and growth of Daphnia cucullata in three hypereutrophic Dutch lakes. Limnol Oceanogr 46:1871–1880

    Article  CAS  Google Scholar 

  • Ederington MC, Mcmanus GB, Harvey HR (1995) Trophic transfer of fatty acids, sterols, and a triterpenoid alcohol between bacteria, a ciliate, and the copepod Acartia tonsa. Limnol Oceanogr 40:860–867

    Article  CAS  Google Scholar 

  • Elser JJ (2002) Biological stoichiometry from genes to ecosystems: ideas, plans, and realities. Integr Comp Biol 42:1226–1326

    Google Scholar 

  • Elser JJ, Hassett RP (1994) A stoichiometric analysis of the zooplankton-phytoplankton interaction in marine and freshwater ecosystems. Nature 370:211–213

    Article  Google Scholar 

  • Flynn KJ, Davidson K (1993) Predator-prey interactions between Isochrysis galbana and Oxyrrhis marina II. Release of nonprotein amines and faeces during predation of Isochrysis. J Plankton Res 15:893–905

    Article  CAS  Google Scholar 

  • Flynn KJ, Davidson K, Cunningham A (1996) Prey selection and rejection by a microflagellate: implications for the study and operation of microbial food webs. J Exp Mar Biol Ecol 196:357–372

    Article  Google Scholar 

  • Frost BW (1972) Effects of size and concentration of food particles on feeding behavior of marine planktonic copepod Calanus pacificus. Limnol Oceanogr 17:805–815

    Article  Google Scholar 

  • Gismervik I (2006) Top-down impact by copepods on ciliate numbers and persistence depends on copepod and ciliate species composition. J Plankton Res 28:499–507

    Article  Google Scholar 

  • Goldman JC, Caron DA, Dennett MR (1987) Nutrient cycling in a microflagellate food chain: IV. Phytoplankton-microflagellate interactions. Mar Ecol Prog Ser 38:75–87

    Article  CAS  Google Scholar 

  • Goldman JC, Dennett MR, Gordin H (1989) Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina. J Plankton Res 11:391–407

    Article  Google Scholar 

  • Gonzalez JM, Sherr EB, Sherr BF (1993) Differential feeding by marine flagellates on growing versus starving, and on motile versus nonmotile, bacterial prey. Mar Ecol Prog Ser 102:257–267

    Article  Google Scholar 

  • Grasshoff K, Kremling K, Ehrhardt M (1999) Methods of seawater analysis. Wiley-VCH, Weinheim

    Book  Google Scholar 

  • Grover JP, Chrzanowski TH (2006) Stoichiometry and growth kinetics in the “smallest zooplankton”—phagotrophic flagellates. Arch Hydrobiol 167:467–487

    Article  CAS  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239

    Article  CAS  Google Scholar 

  • Hammer A, Gruttner C, Schumann R (2001) New biocompatible tracer particles: use for estimation of microzooplankton grazing, digestion, and growth rates. Aquat Microb Ecol 24:153–161

    Article  Google Scholar 

  • Hansen FC, Witte HJ, Passarge J (1996) Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: size selectivity and preference for calcified Emiliania huxleyi cells. Aquat Microb Ecol 10:307–313

    Article  Google Scholar 

  • Hazzard SE, Kleppel GS (2003) Egg production of the copepod Acartia tonsa in Florida Bay: role of fatty acids in the nutritional composition of the food environment. Mar Ecol Prog Ser 252:199–206

    Article  CAS  Google Scholar 

  • Helgen JC (1987) Feeding rate inhibition in crowded Daphnia pulex. Hydrobiologia 154:113–119

    Article  Google Scholar 

  • Hessen DO, Faerovig PJ, Andersen T (2002) Light, nutrients, and P: C ratios in algae: grazer performance related to food quality and quantity. Ecology 83:1886–1898

    Article  Google Scholar 

  • Hessen DO, Agren GI, Anderson TR, Elser JJ, De Ruiter PC (2004) Carbon sequestration in ecosystems: the role of stoichiometry. Ecology 85:1179–1192

    Article  Google Scholar 

  • Howarth RW (1988) Nutrient limitation of net primary production in marine ecosystems. Annu Rev Ecol Syst 19:89–110

    Article  Google Scholar 

  • Jensen TC, Hessen DO (2007) Does excess dietary carbon affect respiration of Daphnia? Oecologia 152:191–200

    Article  Google Scholar 

  • Jeong HJ, Kim JS, Yeong DY, Kim ST, Kim TH, Park MG, Lee CH, Seong KA, Kang NS, Shim JH (2003) Feeding by the heterotrophic dinoflagellate Oxyrrhis marina on the red-tide raphidophyte Heterosigma akashiwo: a potential biological method to control red tides using mass-cultured grazers. J Eukaryot Microbiol 50:274–282

    Article  Google Scholar 

  • Jeong HJ, Song JE, Kang NS, Kim S, Yoo YD, Park JY (2007) Feeding by heterotrophic dinoflagellates on the common marine heterotrophic nanoflagellate Cafeteria sp. Mar Ecol Prog Ser 333:151–160

    Article  Google Scholar 

  • Johnson MP (2000) Physical control of plankton population abundance and dynamics in intertidal rock pools. Hydrobiologia 440:145–152

    Article  Google Scholar 

  • Jonasdottir SH (1994) Effects of food quality on the reproductive success of Acartia tonsa and Acartia hudsonica: laboratory observations. Mar Biol 121:67–81

    Article  Google Scholar 

  • Kimmance SA, Atkinson D, Montagnes DJS (2006) Do temperature-food interactions matter? responses of production and its components in the model heterotrophic flagellate Oxyrrhis marina. Aquat Microb Ecol 42:63–73

    Article  Google Scholar 

  • Klein B, Gieskes WWC, Kraay GG (1986) Digestion of chlorophylls and carotenoids by the marine protozoan Oxyrrhis marina studied by H.P.L.C analysis of algal pigments. J Plankton Res 8:827–836

    Article  CAS  Google Scholar 

  • Kolowith LC, Ingall ED, Benner R (2001) Composition and cycling of marine organic phosphorus. Limnol Oceanogr 46:309–320

    Article  CAS  Google Scholar 

  • Koski M (1999) Carbon: nitrogen ratios of Baltic Sea copepods—indication of mineral limitation? J Plankton Res 21:1565–1573

    Article  Google Scholar 

  • Malzahn AM, Aberle N, Clemmesen C, Boersma M (2007) Nutrient limitation of primary producers affects planktivorous fish condition. Limnol Oceanogr 52:2062–2071

    Article  CAS  Google Scholar 

  • Martin-Creuzburg D, von Elert E (2004) Impact of 10 dietary sterols on growth and reproduction of Daphnia galeata. J Chem Ecol 30:483–500

    Article  CAS  Google Scholar 

  • Nakano S (1994) Carbon: nitrogen: phosphorus ratios and nutrient regeneration of a heterotrophic flagellate fed on bacteria with different elemental ratios. Arch Hydrobiol 129:257–271

    CAS  Google Scholar 

  • Opik H, Flynn KJ (1989) The digestive process of the dinoflagellate Oxyrrhis marina Dujardin feeding on the chlorophyte Dunaliella primolecta Butcher: a combined study of ultrastructure and free amino acids. New Phyt 113:143–151

    Article  CAS  Google Scholar 

  • Pedersen MF, Hansen PJ (2003) Effects of high pH on the growth and survival of six marine heterotrophic protists. Mar Ecol Prog Ser 260:33–41

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Selph KE, Landry MR, Laws EA (2003) Heterotrophic nanoflagellate enhancement of bacterial growth through nutrient remineralization in chemostat culture. Aquat Microb Ecol 32:23–37

    Article  Google Scholar 

  • Skovgaard A (1996) Mixotrophy in Fragilidium subglobosum (Dinophyceae): growth and grazing responses as functions of light intensity. Mar Ecol Prog Ser 143:247–253

    Article  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Sterner RW, Robinson JL (1994) Thresholds for growth in Daphnia magna with high and low phosphorus diets. Limnol Oceanogr 39:1228–1232

    Article  Google Scholar 

  • Strom SL, Benner R, Ziegler S, Dagg MJ (1997) Planktonic grazers are a potentially important source of marine dissolved organic carbon. Limnol Oceanogr 42:1364–1374

    Article  CAS  Google Scholar 

  • Tang KW, Taal M (2005) Trophic modification of food quality by heterotrophic protists: species-specific effects on copepod egg production and egg hatching. J Exp Mar Biol Ecol 318:85–98

    Article  Google Scholar 

  • Tarran GA (1991) Aspects of the grazing behaviour of the marine dinoflagellate Oxyrrhis marina, Dujardin

  • Tillmann U, Reckermann M (2002) Dinoflagellate grazing on the raphidophyte Fibrocapsa japonica. Aquat Microb Ecol 26:247–257

    Article  Google Scholar 

  • Uitto A, Hallfors S (1997) Grazing by mesozooplankton and metazoan microplankton on nanophytoplankton in a mesocosm experiment in the northern Baltic. J Plankton Res 19:655–673

    Article  Google Scholar 

  • Verity PG (1985) Grazing, respiration, excretion, and growth rates of tintinnids. Limnol Oceanogr 30:1268–1282

    Article  Google Scholar 

  • Verity PG (1991) Measurement and simulation of prey uptake by marine planktonic ciliates fed plastidic and aplastidic nanoplankton. Limnol Oceanogr 36:729–750

    Article  Google Scholar 

  • von Elert E (2002) Determination of limiting polyunsaturated fatty acids in Daphnia galeata using a new method to enrich food algae with single fatty acids. Limnol Oceanogr 47:1764–1773

    Article  Google Scholar 

  • Vrede T, Persson J, Aronsen G (2002) The influence of food quality (P: C ratio) on RNA: DNA ratio and somatic growth rate of Daphnia. Limnol Oceanogr 47:487–494

    Article  CAS  Google Scholar 

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Acknowledgments

This study is a part of the PhD studies conducted by F.M.H. at the Biologische Anstalt Helgoland, Alfred-Wegener-Institut Bremerhaven, Germany, financed by GKSS Geesthacht, Germany, and complies with current German law on animal studies. We thank Daniel Schütz, Jacob Hauschildt and Anneke Purz for laboratory assistance and Martin Löder, Christina Gebühr, Katherina Schoo, Petra Brandt, Arne Malzahn and Nils Gülzow for useful discussions. Special thanks to Prof. Dr. Sebastian Diehl and two anonymous reviewers whose suggestions improved the manuscript.

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Correspondence to Florian Matthias Hantzsche.

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Communicated by U.-G. Berninger.

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Hantzsche, F.M., Boersma, M. Dietary-induced responses in the phagotrophic flagellate Oxyrrhis marina . Mar Biol 157, 1641–1651 (2010). https://doi.org/10.1007/s00227-010-1437-1

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