Skip to main content

Advertisement

SpringerLink
Log in

Successful strategies in size structured mixotrophic food webs

  • Published:
Aquatic Ecology Aims and scope Submit manuscript

Abstract

This study investigates how food web structures in aquatic microbial communities emerge based on different mixotrophic life strategies. Unicellular mixotrophic organisms that combine osmotrophy and primary production with phagotrophy account for significant amounts of primary production and bacterivory in marine environments, yet mixotrophs are still usually absent in large-scale biogeochemical models. We here present for the first time a thorough analysis of a food web model with a finely resolved structure in both cell size and foraging mode, where foraging mode is a strategy ranging from pure osmotrophy to pure phagotrophy. A trade-off for maximum uptake rates of mixotrophs is incorporated. We study how different factors determine the food web structure, here represented by the topology of the distribution of given amounts of total phosphorous over the cell size-foraging mode plane. We find that mixotrophs successfully coexist with foraging specialists (pure osmo- and phagotrophs) for a wide range of conditions, a result consistent with the observed prevalence of mixotrophs in recent oceanographic surveys. Mixotrophy trade-off and size-dependent parameters have a strong effect on the emerging community structure, stressing the importance of foraging mode and size considerations when working with microbial diversity and food web dynamics. The proposed model may be used to develop timely representations of mixotrophic strategies in larger biogeochemical ocean models.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aksnes DL, Cao FJ (2011) Inherent and apparent traits in microbial nutrient uptake. Mar Ecol Prog Ser 440:41–51

    Article  Google Scholar 

  • Armstrong RA (2008) Nutrient uptake rate as a function of cell size and surface transporter density: a Michaelis-like approximation to the model of Pasciak and Gavis. Deep Sea Res I 55:1311–1317

    Article  CAS  Google Scholar 

  • Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263

    Article  Google Scholar 

  • Banse K (1982) Cell volumes, maximal growth rates of unicellular algae and ciliates, and the role of ciliates in the marine pelagial. Limnol Ocean 27:1059–1071

    Article  Google Scholar 

  • Baretta-Bekker JG, Barett JW, Hansen AS, Riemann B (1998) An improved model of carbon and nutrient dynamics in the microbial food web in marine enclosures. Aquat Microb Ecol 14:91–108

    Article  Google Scholar 

  • Bjørnsen PK, Kuparinen J (1991) Growth and herbivory by heterotrophic dinoflagellates in the Southern Ocean, studied by microcosm experiments. Mar Biol 109:397–405

    Article  Google Scholar 

  • Burkholder JM, Gilbert PM, Skelton HM (2008) Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8:77–93

    Article  CAS  Google Scholar 

  • Castellani M, Våge S, Strand E, Thingstad F, Giske J (2012) The scaled subspaces method: a new trait-based approach to model communities of populations with largely inhomogeneous density. Ecol Mod. doi:10.1016/j.ecolmodel.2012.12.006

  • Chisholm SW (1992) Primary productivity and biogeochemical cycles in the sea. Plenum Press, Berlin, pp 213–237

  • Crane KW, Grover JP (2010) Coexistence of mixotrophs, autotrophs, and heterotrophs in planktonic microbial communities. J Theor Biol 262:517–527

    Article  PubMed  Google Scholar 

  • Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FJR (2004) The evolution of modern eukaryotic phytoplankton. Science 305:354–360

    Article  PubMed  CAS  Google Scholar 

  • Fenchel T (1982) Ecology of heterotrophic microflagellates. II. Bioenergetics and growth. Mar Ecol Prog Ser 8:225–231

    Article  Google Scholar 

  • Fiksen Ø, Follows MJ, Aksnes DL (2013) Trait-based models of nutrient uptake in microbes extend the Michaelis–Menten framework. Limnol Ocean 58:193–202

    Article  Google Scholar 

  • Flynn KJ, Mitra A (2009) Building the “perfect beast”: modelling mixotrophic plankton. J Plankton Res 31:965–992

    Article  CAS  Google Scholar 

  • Flynn KJ, Stoecker DK, Mitra A, Rave JA, Glibert PM, Hansen PJ, Graneli E, Burkholder JM (2013) Misuse of the phytoplantkon–zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton funktional types. J Plankton Res 35:3–11

    Article  Google Scholar 

  • Friebele ES, Correl DL, Faust MA (1978) Relationship between phytoplankton cell size and the rate of orthophosphate uptake: in situ observations of an estuarine population. Mar Biol 45:39–52

    Article  CAS  Google Scholar 

  • Guildford SJ, Hecky RE (2000) Total nitrogen, total phosphorus, and nutrient limitation in lakes and oceans: is there a common relationship?. Limnol Ocean 45:1213–1223

    Article  CAS  Google Scholar 

  • Hammer AC, Pitchford JW (2005) The role of mixotrophy in plankton bloom dynamics, and the consequences for productivity. ICES J Mar Sci 62:833–840

    Article  Google Scholar 

  • Hansen B, Bjørnsen PK, Hansen PJ (1994) The size ratio between planktonic predators and their prey. Limnol Ocean 39:395–403

    Article  Google Scholar 

  • Hansen PJ, Bjørnsen PK, Hansen BW (1997) Zooplankton grazing and growth: scaling within the 2–2,000-μm body size range. Limnol Ocean 42:687–704

    Article  Google Scholar 

  • Hartmann M, Grub C, Tarran GA, Martin AP, Burkill PH, Scanlan DJ, Zubkov MV (2012) Mixotrophic basis of Atlantic oligotrophic ecosystems. PNAS USA 109:5756–5760

    Article  PubMed  CAS  Google Scholar 

  • Havskum H, Riemann B (1996) Ecologcial importance of bacterivorous, pigmented flagellates (mixotrophs) in the Bay of Aarhus, Denmark. Mar Ecol Prog Ser 137:251–263

    Article  Google Scholar 

  • Irwin AJ, Finkel ZV, Schofield OME, Falkowski PG (2006) Scaling-up from nutrient physiology to the size-structure of phytoplankton communities. J Plankton Res 28:459–471

    Article  Google Scholar 

  • Jones RI (1997) A classification of mixotrophic protists based on their behaviour. Freshw Biol 37:35–43

    Article  Google Scholar 

  • Jost C, Lawrence CA, Campolongo F, van de Bund W, Hill S, DeAngelis DL (2004) The effects of mixotrophy on the stability and dynamics of a simple planktonic food web model. Theor Popul Biol 66:37–51

    Article  PubMed  Google Scholar 

  • Jumars P, Deming J, Hill P, Karp-Boss L, Dade W (1993) Physical constraints on marine osmotrophy in an optimal foraging context. Mar Microb Food Webs 7:121–161

    Google Scholar 

  • Kemp PF, Lee S, LaRoche J (1993) Estimating the growth rate of slowly growing marine bacteria from RNA content. Appl Environ Microbiol 59:2594–2601

    PubMed  CAS  Google Scholar 

  • Krom MD, Woodward EMS, Herut B, Kress N, Carbo P, Mantoura RFC, Spyres G, Thingstad TF, Wassmann P, Wexels-Riser C, Kitidis V, Law CS, Zoda G (2005) Nutrient cycling in the south east Levantine basin of the eastern Mediterranean: results from a phosphorous starved system. Deep Sea Res II 52:2879–2896

    Article  Google Scholar 

  • Laflamme M, Xiao S, Kowalewski M (2009) Osmotrophy in modular Ediacara organisms. PNAS USA 106:14438–14443

    Article  CAS  Google Scholar 

  • Lignell R, Haario H, Laine M, Thingstad TF (2013) Getting the “right” parameter values for models of the pelagic microbial food web. Limnol Ocean 58:301–313

    Article  CAS  Google Scholar 

  • Litchman E, Klausmeier CA, Schofield OM, Falkowski PG (2007) The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecol Lett 10:1170–1181

    Article  Google Scholar 

  • Loeuille N, Loreau M, Levin SA (2005) Evolutionary emergence of size-structure food webs. PNAS USA 102:5761–5766

    Article  PubMed  CAS  Google Scholar 

  • Maranon E, Behrenfeld MJ, Gonzalez N, Mourino B, Zubkov MV (2003) High variability of primary production in oligotrophic waters of the Atlantic Ocean: uncoupling from phytoplankton biomass and size structure. Mar Ecol Prog Ser 257:1–11

    Article  Google Scholar 

  • McKie-Kriesberg ZM, Fay SA, Sanders RW (2011) Competitive assays of two mixotrophs and two diatoms from the Ross Sea, Antarctica. J Phycol 47:S67–S67

    Google Scholar 

  • Mitra A, Flynn KJ (2010) Modelling mixotrophy in harmful algal blooms: more or less the sum of the parts? J Mar Syst 83:158–169

    Article  Google Scholar 

  • Moloney CL, Field JG (1991) The size-based dynamics of plankton food webs. I. A simulation model of carbon and nitrogen flows. J Plankton Res 13:1003–1038

    Article  Google Scholar 

  • Pitta P, Stambler N, Tanaka T, Zohary T, Tselepides A, Rassoulzadegan F (2005) Biological response to P addition in the Eastern Mediterranean Sea. The microbial race against time. Deep Sea Res II 52:2961–2974

    Article  CAS  Google Scholar 

  • Pomeroy LR, Wiebe WJ (1988) Energetics of microbial food webs. Hydrobiologia 159:7–18

    Article  Google Scholar 

  • Psarra S, Zohary T, Krom MD, Mantoura RFC, Polychronaki T, Stambler N, Tanaka T, Tselepides A, Thingstad TF (2005) Phytoplankton response to a Lagrangian phosphate addition in the Levantine Sea (Eastern Mediterranean). Deep Sea Res II 52:2944–2960

    Article  CAS  Google Scholar 

  • Raven JA (1998) The twelfth Tansley lecture, small is beautiful: the picophytoplankton. Funct Ecol 12:503–513

    Article  Google Scholar 

  • Rothhaupt KO (1996) Utilization of substitutable carbon and phosphorus sources by the mixotrophic chrysophyte ochromonas sp. Ecology 77:706–715

    Article  Google Scholar 

  • Sanders RW (1991) Mixotrophic protists in marine and freshwater ecosystems. J Eukaryot Microbiol 38:76–81

    Article  Google Scholar 

  • Sanders RW (2011) Alternative nutritional strategies in protists: symposium introduction and a review of freshwater protists that combine photosynthesis and heterotrophy. J Eukaryot Microbiol 58:181–184

    Article  Google Scholar 

  • Sanders RW, Porter KG, Caron DA (1990) Relationship between phototrophy and phagotrophy in the mixotrophic chrysophyte Poteriochromonas malhamensis. Microb Ecol 19:97–109

    Article  Google Scholar 

  • Sanders RW, Berninger UG, Lim EL, Kemp PF (2000) Heterotrophic and mixotrophic nanoplankton predation on picoplankton in the Sargasso Sea and on Georges Bank. Mar Ecol Prog Ser 192:103–118

    Article  Google Scholar 

  • Shampine LF, Reichelt MW (1997) The matlab ODE suite. SIAM J Sci Comput 18:1–22

    Article  Google Scholar 

  • Sheldon RW, Prakash A, Sutcliffe WH (1972) The size distribution of particles in the ocean. Limnol Ocean 17:327–340

    Article  Google Scholar 

  • Stickney HL, Hood RR, Stoecker DK (2000) The impact of mixotrophy on planktonic marine ecosystems. Ecol Mod 125:203–230

    Article  CAS  Google Scholar 

  • Stockner JG, Shortreed KS (1989) Algal picoplankton production and contribution to food-webs in oligotrophic Brititsh Columbia lakes. Hydrobiologia 173:151–166

    Article  CAS  Google Scholar 

  • Stoecker DK (1998) Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. Eur J Protistol 34:281–290

    Article  Google Scholar 

  • Stoecker DK (1999) Mixotrophy among dinoflagellates. J Eukaryot Microbiol 46:397–401

    Article  Google Scholar 

  • Stoecker DK, Taniguchi A, Michaels AE (1989) Abundance of autotrophic, mixotrophic and heterotrophic planktonic ciliates in shelf and slope waters. Mar Ecol Prog Ser 50:241–254

    Article  Google Scholar 

  • Suttle CA, Harrison PJ (1988) Ammonium and phosphate uptake rates, N:P supply ratios, and evidence for N and P limitation in some oligotrophic lakes. Limnol Ocean 33:186–202

    Article  CAS  Google Scholar 

  • Tambi H, Flaten GAF, Egge JK, Bødtker G, Jacobsen A, Thingstad TF (2009) Relationship between phosphate affinities and cell size and shape in various bacteria and phytoplankton. Aquat Microb Ecol 57:311–320

    Article  Google Scholar 

  • Taylor WD (1978) Growth responses of ciliate protozoa to the abundance of their bacterial prey. Microb Ecol 4:207–214

    Article  Google Scholar 

  • Thingstad TF, Havskum H, Garde K, Riemann B (1996) On the strategy of “eating your competitor”: a mathematical analysis of algal mixotrophy. Ecology 77:2108–2118

    Article  Google Scholar 

  • Thingstad TF, Krom MD, Flagen GAF, Mantoura RFC, Groom S, Herut B, Kress N, Law CS, Pasternak A, Pitta P, Psarra S, Rassoulzadegan R, Tanaka T, Tselepides A, Wassmann P, Woodward EMS, Riser CW, Zodiatis G, Zohary T (2005a) Nature of phosphorous limitation in the ultraoligotrophic Eeastern Mediterranean. Science 309:1068–1071

  • Thingstad TF, Øvreås L, Egge JK, Løvdal T, Heldal M (2005b) Use of non-limiting substrates to increase size; a generic strategy to simultaneously optimize uptake and minimize predation in pelagic osmotrophs?. Ecol Lett 8:675–682

    Article  Google Scholar 

  • Troost TA, Kooi BW, Kooijman SALM (2005) When do mixotrophs specialize? Adaptive dynamics theory applied to a dynamic energy budget model. Math Biosci 193:159–182

    Article  PubMed  Google Scholar 

  • Unrein F, Massana R, Alonso-Sáez L, Gasol JM (2007) Significant year-round effect of small mixotrophic flagellates on bacterioplankton in an oligotrophic coastal system. Limnol Ocean 52:456–469

    Article  Google Scholar 

  • Vaqué D, Gasol JM, Marrasé C (1994) Grazing rates on bacteria: the significance of methodology and ecological factors. Mar Ecol Prog Ser 109:263–274

    Article  Google Scholar 

  • Ward BA, Dutkiewicz S, Barton AD, Follows MJ (2011) Biophysical aspects of resource acquisition and competition in algal mixotrophs. Am Nat 178:98–112

    Article  PubMed  Google Scholar 

  • Zhang Q, Gradinger R, Spindler M (1998) Dark survival of marine microalgae in the high Arctic (Greenland Sea). Polarforschung 65:111–116

    Google Scholar 

  • Zohary T, Herut B, Krom MD, Mantoura RFC, Pitta P, Psarra S, Rassoulzadegan F, Stambler N, Tanaka T, Thingstad TF, Woodward EMS (2005) P-limited bacteria but N and P co-limited phytoplankton in the Eastern Mediterranean—a microcosm experiment. Deep Sea Res II 52:3011–3023

    Article  Google Scholar 

  • Zubkov MV, Tarran GA (2008) High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455:224–227

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The study was done as part of the MINOS project financed by EU-ERC (proj.nr 250254) and with the support of the Norwegian Research Council. We thank two anonymous reviewers for constructive comments that improved a previous version of the manuscript.

Author information

Authors and Affiliations

  1. Department of Biology, University of Bergen, 5020, Bergen, Norway

    Selina Våge, Marco Castellani, Jarl Giske & T. Frede Thingstad

Authors
  1. Selina Våge
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marco Castellani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jarl Giske
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. Frede Thingstad
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Selina Våge.

Additional information

Handling Editor: Piet Spaak.

Electronic supplementary material

Below is the link to the electronic supplementary material.

RTF (1 KB)

Electronic supplementary material

Below is the link to the electronic supplementary material.

M (4 KB)

Electronic supplementary material

Below is the link to the electronic supplementary material.

M (3 KB)

Electronic supplementary material

Below is the link to the electronic supplementary material.

M (14 KB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Våge, S., Castellani, M., Giske, J. et al. Successful strategies in size structured mixotrophic food webs. Aquat Ecol 47, 329–347 (2013). https://doi.org/10.1007/s10452-013-9447-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10452-013-9447-y

Keywords

Search

Navigation