Big fish eat small fish: implications for food chain length?

Abstract

Food chains in the pelagic zones of oceans and lakes are longer than in terrestrial ecosystems. The perception of the pelagic food web has become increasingly complex by progressing from a linear food chain (phytoplankton — crustacean zooplankton — planktivorous fish — predatory fish) to a food web because of an increasing appreciation of microbial trophic pathways, side-tracks by gelatinous zooplankton and a high prevalence of omnivory. The range of predator:prey size ratios by far exceeds the traditionally assumed range of 10:1 to 100:1, from almost equal length to 105:1. The size ratios between primary consumers and top predators are 3½ orders of magnitude bigger in pelagic than in terrestrial food webs. Comparisons between different pelagic ecosystems support ecosystem size as an important factor regulating the maximal trophic level, while energy limitation of the number of trophic levels is less well supported. An almost 1:1 relationship between ingestion by predators and prey mortality and a better chemical match between primary producer and herbivore biomass are further distinctive features of the pelagic food web whose role in explaining the higher number of trophic levels in pelagic systems needs further examination.

Abbreviations

DOC:

Dissolved Organic Carbon

HNF:

Heterotrophic NanoFlagellates

NP:

Nekton Production

PP:

Primary Production

TL:

Trophic Level

References

  1. Aberle, N., A.M. Malzahn, Lewandowska, A. and U. Sommer. 2014. Some like it hot – the protozooplankton – copepod link in a warming ocean. Mar. Ecol. Progr. Ser. 519:103–112.

    Article  Google Scholar 

  2. Azam, F., T. Fenchel. J.G. Field, J.S. Gray, L.A. Meyer-Reil and F. Thingstad. 1983. The ecological role of water column microbes in the sea. Mar. Ecol. Progr. Ser. 10:257–263.

    Article  Google Scholar 

  3. Baird, D. and R.E. Ulanowicz. 1989. The seasonal dynamics of the Chesapeake Bay ecosystem. Ecol. Monogr. 59:329–364.

    Article  Google Scholar 

  4. Båmstedt, U., M.B. Martinussen and S. Matsakis. 1994. Trophodynamics of the 2 scyphozoan jellyfishes, Aurelia aurita and Cyanea capillata in western Norway. ICES J. Mar. Sci. 51:369–382.

    Article  Google Scholar 

  5. Basedow, S.L., N.A.L. de Silva, A. Bode and J. van Beusekom. 2016. The trophic positions of mesozooplankton across the North Atlantic: estimates derived from biovolume theories and stable isotope analysis. J. Plankton Res. 38:1364–1378.

    CAS  Google Scholar 

  6. Bedo, A., L. Acuña, D. Robin and R. Harris. 1993. Grazing in the micron and the sub-micron particle size range: the case of Oikopleura dioica (Appendicularia). Bull. Mar. Sci. 53:2–14.

    Google Scholar 

  7. Bird, D.F. and J. Kalff. 1987. Algal phagotrophy: regulating factors and importance relative to photosynthesis in Dinobryon. Limnol Oceanogr. 32:277–284.

    Article  CAS  Google Scholar 

  8. Boenigk, J. and H. Arndt. 2002. Bacterivory by heterotrophic flagellates: community structure and feeding strategies. Antonie van Leeuwenhoek 81:465–480.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Brandt, S.M. and M.A. Sleigh. 2000. The quantitative occurrence of different taxa of heterotrophic flagellates in Southampton Water, U.K. Estuar. Coast. Shelf Sci. 51:91–102.

    Article  Google Scholar 

  10. Briand, F. and J.E. Cohen. 1987. Environmental correlates of food chain length. Science 238:956–960.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Calbet, A., M.R. Landry and S. Nunnery. 2001. Bacteria-flagellate interactions in the microbial food web of the oligotrophic subtropical North Pacific. Aqu. Microb. Ecol. 23:283–292.

    Article  Google Scholar 

  12. Calbet, A. and M. Landry. 2004. Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol. Oceanogr. 49:51–57.

    Article  CAS  Google Scholar 

  13. Caron, D.A., H.G. Dam, P. Kremer, E.J. Lessard EJ, L.P. Madin, T.C. Malone, J.M. Napp, E.R. Peele, M.R. Roman and M.J. Youngbluth. 1995. The contribution of microorganisms to particulate carbon and nitrogen in surface waters of the Sargasso Sea near Bermuda. Deep-Sea Res. I 42:943–972.

    Article  CAS  Google Scholar 

  14. Cohen, J.E., S.L. Pimm, P. Yodzis and J. Saldana. 1993. Body size of animal predators and animal prey in food webs. J. Anim. Ecol. 62:67–78.

    Article  Google Scholar 

  15. Deibel, D. 1982. Laboratory-measured grazing and ingestion rates of the salp, Thalia democratica Forskal, and the doliolid, Dolioletta gegenbauri Uljanin (Tunicata, Thaliacea). J. Plankton Res. 4: 189–201.

    Article  Google Scholar 

  16. Elser J.J., W.F. Fagan, R.F. Denno, D.R. Dobberfuhl, A. Folarin, A. Huberty, S. Interlandi, S.S. Kilham, E. McCauley, K.L. Schulz, E.H. Siemann and R.W. Sterner. 2000. Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578580.

    Article  CAS  Google Scholar 

  17. Elton, C.S. 1927. Animal Ecology. Macmillan, New York.

    Google Scholar 

  18. Fernández, D., Á. López-Urrutia, A. Fernández, J-L. Acuña and R. Harris R. 2004. Retention efficiency of 0.2 to 6 μm particles by the appendicularians Oikopleura dioica and Fritillaria borealis. Mar. Ecol. Prog. Ser. 266:89–101.

    Article  Google Scholar 

  19. Goldman, J.C., J.J. McCarthy and D.G. Peavey. 1979. Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature 279:210–215.

    Article  CAS  Google Scholar 

  20. Hairston Jr., N.G. and N.G. Hairston Sr. 1993. Cause-effect relationships in energy flow, trophic structure and interspecific interactions. Am. Nat. 142 379–411.

    Article  Google Scholar 

  21. Hairston Jr., N.G and N.G. Hairston Sr. 1997. Does food web complexity eliminate trophic level dynamics? Am. Nat. 149:1001–1007.

    Article  Google Scholar 

  22. Hansen, B., P-K. Bjørnsen and P.J. Hansen. 1994. The size ratio between planktonic predators and their prey. Limnol. Oceanogr. 39:395–403.

    Article  Google Scholar 

  23. Hansen, P.J. 2011. The role of photosynthesis and food uptake for the growth of marine mixotrophic dinoflagellates. J. Eukaryot. Microbiol. 58:203–214.

    Article  CAS  Google Scholar 

  24. Hansen, T., A. Burmeister and U. Sommer. 2009. Simultaneous δ15N, δ13 C and δ34 S abundance measurements of low biomasses using a technical advanced high sensitivity elemental analyzer connected to an isotope ratio mass spectrometer. Rap. Comm. Mass Spectrometry 23:3387–3393.

    Article  CAS  Google Scholar 

  25. Holt, R.D. and G.A. Polis. 1997. A theoretical framework for intraguild predation. Am. Nat. 149:745–764.

    Article  Google Scholar 

  26. Hunt, B. P.V., V. Allain, C. Menkes, A. Lorrain, B. Graham, M. Rodier, M. Pagano and F. Carlotti. 2015. A coupled stable isotope-size spectrum approach to understanding pelagic food-web dynamics: a case study from the southwest sub-tropical Pacific. Deep Sea Res. Part II 113:208–224

    Article  CAS  Google Scholar 

  27. Hussey, N.E., M.A. MacNeill, B.C. McMeans, J.A. Olin, S.F.J. Dudley, G. Cliff, S.P. Wintner, S.T. Fennesy and A.T. Fisk. 2014. Rescaling the trophic structure of marine food webs. Ecol. Lett. 17:239–250.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Ismar, S.M.H., J. Kottmann and U. Sommer. 2018. First genetic quantification of sex- and stage-specific feeding in the ubiquitous copepod Acartia tonsa. Mar. Biol. Submitted.

  29. Iverson, R.L. 1990. Control of marine fish production. Limnol. Oceanogr. 35:1593–1594.

    Article  Google Scholar 

  30. Jones, R.I. 2000. Mixotrophy in planktonic protist. An overview. Freshwater Biol. 45:219–226.

    Article  Google Scholar 

  31. Katechakis, A., H. Stibor, U. Sommer and T. Hansen. 2004. Feeding selectivities and food niche separation of Acartia clausi, Penilia avirostris (Crustacea) and Doliolum denticulatum (Thaliacea) in Blanes Bay (Catalan Sea, NW Mediterranean). J. Plankton Res. 26:589–603.

    Article  Google Scholar 

  32. Leaper, R. and M. Huxham. 2002. Size constraints in a real food web: predator, parasite and prey body-size relationships. Oikos 99:443–456.

    Article  Google Scholar 

  33. Lindeman, R.L. 1942. The trophodynamic aspect of ecology. Ecology 23:399–417.

    Article  Google Scholar 

  34. Marañón, E. 2015. Cell size as a key determinant of phytoplankton metabolism and community structure. Ann. Rev. Mar. Sci. 7:241–264.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Marañón, E., P. Cermeño, M. Latasa and R.D. Tadonleke. 2015. Resource supply alone explains the variability of marine phytoplankton size structure. Limnol. Oceanogr. 60:1848–1854.

    Article  Google Scholar 

  36. McCann, K. and A. Hastings. 1997. Re-evaluating the omnivorystability relationship in food webs. Proc. R. Soc. Lond. Ser. B. 264:186–193.

    Article  Google Scholar 

  37. McGarvey, R., N. Dowling and J.E. Cohen. 2016. Longer food chains in pelagic ecosystems. Trophic energetics of animal body size and metabolic efficiency. Am. Nat. 188:76–86.

    PubMed  PubMed Central  Google Scholar 

  38. Miller, R.J., K.H. Mann and D.J. Scarrat. 1971. Potential primary production of a lobster-seaweed community in eastern Canada. J. Fish. Res. Bd. Can. 28:1733–1738.

    Article  Google Scholar 

  39. Moustaka-Gouni, M., K.A. Kormas, M. Scotti, E. Vardaka and U. Sommer. 2016. Warming and acidification effects on planktonic heterotrophic pico- and nanoflagellates in a mesocosm experiment. Protist 167:389–410.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Pimm, S.L. 1980. Properties of food webs. Ecology 61:219–225.

    Article  Google Scholar 

  41. Pimm, S.L. 1982. Food Webs. Chapman and Hall, London.

    Book  Google Scholar 

  42. Polis, G.A. and D.R. Strong. 1996. Food web complexity and community dynamics. Am. Nat. 147:813–846.

    Article  Google Scholar 

  43. Pomeroy, L.R. 1974. The ocean foodweb, a changing paradigm. BioScience 24:499–504.

    Article  Google Scholar 

  44. Post, D.M., M.L. Pace ML and N.G. Hairston Jr. 2000. Ecosystem size determines food-chain length in lakes. Nature 405:1047–1049.

    Article  CAS  Google Scholar 

  45. Samuelsson, K. and A. Andersson. 2003. Predation limitation in the pelagic microbial food web in an oligotrophic aquatic system. Aquat. Microb. Ecol. 30:239–250.

    Article  Google Scholar 

  46. Schoener, T.W. 1989. Food webs from the small to the large. Ecology 70:1559–1589.

    Article  Google Scholar 

  47. Scotti, M., S. Allesina, C. Bondavalli, A. Bodini and L.G. Abarca-Arenas. 2006. Effective trophic positions in ecological acyclic networks. Ecol. Model. 198:495–505.

    Article  Google Scholar 

  48. Scotti, M., C. Bondavalli, A. Bodini and S. Allesina. 2009. Using trophic hierarchy to understand food web structure. Oikos 118:1695–1702.

    Article  Google Scholar 

  49. Sherr, E.B. and B.F. Sherr. 2002. Significance of predation by protists in aquatic microbial food webs. Antonie van Leeuwenhoek 81:293–308.

    Article  CAS  Google Scholar 

  50. Shurin, J.B., D.S. Gruner and H. Hillebrand. 2006. All wet or dried up? Real differences between aquatic and terrestrial food webs. Proc. R. Soc. B. 273:1–9.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Sieburth, J.M., V. Smetacek, V. and J. Lenz. 1978. Pelagic ecosystem structure: heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnol. Oceanogr. 23:1256–1263.

    Article  Google Scholar 

  52. Sommer, U., E. Charalampous, S. Genitsaris and M. Moustaka-Gouni. 2017. Costs, benefits and taxonomic distribution of phytoplankton body size. J. Plankton Res. 39:494–508.

    CAS  Google Scholar 

  53. Sommer, U., T. Hansen, O. Blum, N. Holzner, O. Vadstein and H. Stibor. 2005. Copepod and microzooplankton grazing n mesocosms fertilised with different Si:N ratios: no overlap between food spectra and Si:N-influence on zooplankton trophic level. Oecologia 142:274–283.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Sommer, U. and F. Sommer. 2006. Cladocerans versus copepods: the cause of contrasting top-down controls on freshwater and marine phytoplankton. Oecologia 147:183–194.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Sommer, U., F. Sommer, H. Feuchtmayr and T. Hansen. 2004. The influence of mesozooplankton on phytoplankton nutrient limitation: A mesocosm study with northeast Atlantic phytoplankton. Protist 155:295–304.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Sommer, U., H. Stibor, A. Katechakis, F. Sommer and T. Hansen. 2002. Pelagic food web configurations at different levels of nutrient richness and their implications for the ratio fish production:primary production. Hydrobiologia 484:11–20.

    Article  Google Scholar 

  57. Stibor, H. and U. Sommer. 2003. Mixotrophy of a photosynthetic flagellate viewed from an optimal foraging perspective. Protist 154:91–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Tait, R.V. 1981. Elements of Marine Ecology. 3rd ed. Butterworths, London.

  59. Thingstad, T.F., H. Havskum, K. Garde and B. Riemann. 1996. On the strategy of “eating your competitor”: a mathematical analysis of algal mixotrophy. Ecology 77:2108–2118.

    Article  Google Scholar 

  60. Thompson, R.M., M. Hemberg, B.M. Starzomski and J.B. Shurin. 2007. Trophic levels and trophic tangles: the prevalence of omnivory in real food webs. Ecology 88:612–617.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Vander Zanden, M.J., B.J. Shuter, N. Lester and J.B. Rasmussen. 1999. Patterns of food chain length in lakes: A stable isotope study. Am. Nat. 154:406–416.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Whittaker, R.H. 1975. Communities and Ecosystems. 2nd ed., Macmillan, New York.

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to U. Sommer.

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sommer, U., Charalampous, E., Scotti, M. et al. Big fish eat small fish: implications for food chain length?. COMMUNITY ECOLOGY 19, 107–115 (2018). https://doi.org/10.1556/168.2018.19.2.2

Download citation

Keywords

  • Body size
  • Food web
  • Nekton
  • Pelagic
  • Plankton
  • Trophic level