Aquatic Ecology

, Volume 40, Issue 3, pp 391–405 | Cite as

Relationships between fish feeding guild and trophic structure in English lowland shallow lakes subject to anthropogenic influence: implications for lake restoration

  • Luis ZambranoEmail author
  • Martin R. Perrow
  • Carl D. Sayer
  • Mark L. Tomlinson
  • Thomas A. Davidson
Original Paper


The shallow lakes of Eastern England have been subject to intense anthropogenic pressures including nutrient enrichment and fish stocking. We sought to determine the relationships between fish community structure and other ecosystem characteristics in 28 of these lakes through classification of fish species into piscivorous, zooplanktivorous and benthivorous feeding guilds according to the literature. Canonical correspondence analysis produced clear associations between fish and ecosystem characteristics that generally agreed with other theoretical (e.g. the alternative stable states hypothesis) and empirical studies, but with some important differences. There was a striking lack of relationships between nutrients and other variables, indicating the importance of top-down rather than bottom-up processes as a structuring force in the generally eutrophic study lakes. The presence of submerged (and shoreline) vegetation was associated with a diverse assemblage of apparently co-existing piscivorous (principally pike Esox lucius) and zooplanktivorous species. Perch Perca fluviatilis, a significant predator in other studies, was unimportant and argued to be limited by water quality in the extremely shallow lakes. In contrast, the benthivorous fish guild (principally carp Cyprinus carpio, bream Abramis brama and tench Tinca tinca) essentially represented the inverse of the potential pelagic associations between piscivores/zooplanktivores and vegetation. The introduction of large benthivores to many study lakes could have precipitated a loss of submerged vegetation through direct uprooting during foraging, with the effect of simplifying the fish community being most acute where littoral vegetation was limited by other anthropogenic factors. It is implied that attempts to promote or restore submerged vegetation in these lakes would best target benthivorous species.


Feeding guild Trophic interactions Submerged macrophytes Benthivorous fish Zooplanktivorous fish Piscivorous fish Lake management and conservation 


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We are thankful for the kind permission of many landowners, land managers/gamekeepers who gave us access to lakes on their property. Thanks also to Eduardo Pérez García and several anonymous referees for their comments on the manuscript. This research was funded by a NERC fellowship (GT5/98/21/CB) and a NERC small grant (GR8/4350) awarded to C. Sayer.


  1. Adamek Z, Sukop I, Moreno Rendón P, Kouril J (2003) Food competition between 2+ tench (Tinca tinca L.), common carp (Cyprinus carpio L.) and bigmouth buffalo (Ictiobus cyprinellus Val.) in pond polyculture. J Appl Ichthyol 19:165–169CrossRefGoogle Scholar
  2. Bergman E (1991) Changes in abundance of two percids, Perca fluviatilis and Gymnocephalus cernuus along a productivity gradient. Can Fish Aquat Sci 48:536–545CrossRefGoogle Scholar
  3. Beyerle GB, Williams JE (1968) Some observations of food selectivity by northern pike in aquaria. Trans Am Fish Soc 97:28–31CrossRefGoogle Scholar
  4. Bird DJ, Cowx I (1993) The selection of suitable pulsed currents for electric fishing in fresh waters. Fish Res 18:363–376CrossRefGoogle Scholar
  5. Bohl E (1982) Food supply and prey selection in planktivorous Cyprinidae. Oecologia 53:134–138CrossRefGoogle Scholar
  6. Borcherding J, Maw SK, Tauber S (2000) Growth of 0+ perch␣(Perca fluviatilis) predating on 0+ bream (Abramis brama). Ecol Freshw Fish 9:236–241CrossRefGoogle Scholar
  7. Brabrand Å (1995) Intra-cohort cannibalism among larval stages of perch (Perca fluviatilis). Ecol Freshw Fish 4: 70–76CrossRefGoogle Scholar
  8. Breukelaar AW, Lammens EHRR, Breteler JGPK, Tatrai I (1994) Effects of benthivorous bream (Abramis brama) and carp (Cyprinus carpio) on sediment resuspension and concentrations of nutrients and chlorophyll a. Freshw Biol 32:113–121CrossRefGoogle Scholar
  9. Brodgar, 2.2.8., (2004). Software package for multivariate analysis and multivariate time series analysis. Highland Statistics Ltd. www.brodgar.comGoogle Scholar
  10. Brönmark C, Weisner SEB (1992) Indirect effects of fish community structure on submerged vegetation in shallow, eutrophic lakes: An alternative mechanism. Hydrobiologia 243/244:293–301CrossRefGoogle Scholar
  11. Bry C (1996). Role of vegetation in the life cycle of pike. In:␣Craig JF (ed) pike—Biology and exploitation, Chapman & Hall, Fish and Fisheries Series, 19 London, UK, pp 45–67Google Scholar
  12. Bucke D (1971) The anatomy and histology of the alimentary tract of the carnivorous fish the pike Esox lucius L. J Fish Biol 3:421–431CrossRefGoogle Scholar
  13. Canfield D, Shireman J, Colle D, Haller W, Watkins CE, Maceina M (1984) Prediction of chlorophyll-a concentrations in Florida lakes: importance of aquatic macrophytes. Can J Fish Aquat Sci 41:497–501CrossRefGoogle Scholar
  14. Carvalho L, Moss B (1995) The current status of a sample of English Sites of special Scientific Interest subject to eutrophication Aquatic conservation. Mar Freshw Ecosyst 5:191–204CrossRefGoogle Scholar
  15. Collette B, Ali MA, Hokanson KEF, Nagiec M, Smirnov SA, Thorpe JE, Weatherley AH (1977) Biology of the percids. J Fish Res Board Canada 34:1890–1899Google Scholar
  16. Copp GH, Peñáz M (1988) Ecology of fish spawning and nursery zones in the flood plain, using a new sampling approach. Hydrobiologia 169:209–224Google Scholar
  17. Crivelli AJ (1983) The destruction of aquatic vegetation by carp Cyprinus carpio a comparison between southern France and the USA. Hydrobiologia 106:37–42CrossRefGoogle Scholar
  18. Cryer M, Peirson G, Townsend CR (1986) Reciprocal interactions between roach, Rutilus rutilus and zooplankton in a shallow lake: prey dynamics and fish growth and recruitment. Limnol Oceanogr 31:1022–1038CrossRefGoogle Scholar
  19. Declerck S, Louette G, De Bie T, De Meester L (2002) Patterns␣of diet overlap between populations of non-indigenous and native fishes in shallow ponds. J Fish Biol 61:1182–1197CrossRefGoogle Scholar
  20. Diehl S (1988) Foraging efficiency of three freshwater fishes:␣Effects of structural complexity and light. Oikos 53:207–214CrossRefGoogle Scholar
  21. Diehl S, Kornijów R (1998) Influence of submerged macrophytes on trophic interactions among fish and macroinvertebrates. In: Jeppesen E, Søndergaard Ma, Søndergaard Mo, Christoffersen K (eds) The structuring role of submerged macrophytes in lakes. Ecological Studies Series Springer Verlag, New York, pp 24–46Google Scholar
  22. Dörner H, Soren B, Jacobsen L, Hülsmann S, Brojerg M, Wagner A (2003) The feeding behaviour of large perch Perca fluviatilis (L.) in relation to food availability: a comparative study. Hydrobiologia 506–509:427–434CrossRefGoogle Scholar
  23. Flik BJG, Vijverberg J (2003) Contrasting migration behaviour of Daphnia pulicaria and D. galeata × hyalina, in avoidance of predation by 0+perch (Perca fluviatilis). Hydrobiologia 491:289–299CrossRefGoogle Scholar
  24. Garcia-Berthou E, Moreno-Amich R (2000) Rudd (Scardinius erythrophthalmus) introduced to the Iberian Peninsula: feeding ecology in Lake Banyoles. Hydrobiologia 436:159–164CrossRefGoogle Scholar
  25. Golani D, Shefler D, Gelman A (1998) Aspects of growth and feeding habits of the adult European eel (Anguilla anguilla) in Lake Kinneret (Lake Tiberias), Israel. Aquaculture 74:349–354CrossRefGoogle Scholar
  26. Grimm MP (1983) Regulation of biomasses of small (<41 cm) Northern pike (Esox lucius L.) with special reference to the contribution of individuals stocked as fingerlings. Fish Manag 14:115–134Google Scholar
  27. Hayek CL-A, Buzas MA (1997) Surveying Natural Populations. Columbia University Press, N.YGoogle Scholar
  28. Hyvärinen P, Vehanen T (2004) Effect of brown trout body size on post-stocking survival and pike predation. Ecol Freshw Fish 13:77–84CrossRefGoogle Scholar
  29. Jacobsen L, Perrow MR, Landkildehus F, Hjørne M, Lauridsen TL, Berg S (1997) Interactions between piscivores, zooplanktivores and zooplankton in submerged macrophytes: Preliminary observations from enclosure and pond experiments. Hydrobiologia 342/343:197–205CrossRefGoogle Scholar
  30. Jacobsen L, Perrow MR (1998) Predation risk from piscivorous fish influencing the diel use of macrophytes by planktivorous fish in experimental ponds. Ecol Freshw Fish 7:78–86CrossRefGoogle Scholar
  31. Jeppesen E, Sammalkarpi I (2002) Lakes. In: MR Perrow, Davy AJ (eds) Handbook of ecological restoration, vol 2. Restoration in Practice. Cambridge University Press, Cambridge, UK, pp 297–324Google Scholar
  32. Jeppesen E, Lauridsen TL, Kairesalo T, Perrow MR (1998) Impact of submerged macrophytes on fish-zooplankton interactions in lakes. In: Jeppesen E, Søndergaard Ma, Søndergaard Mo, Christoffersen K (eds) The structuring role of submerged macrophytes in lakes. Ecological Studies Series, Springer Verlag, New York, pp 91–114Google Scholar
  33. Jeppesen E, Jensen JP, Søndergaard M, Lauridsen T, Landkildehus F (2000) Trophic structure. species richness and biodiversity in Danish lakes: changes along a phosphorus gradient. Freshw Biol 45:201–218CrossRefGoogle Scholar
  34. Johnes P, Heathwaite A (1992) A procedure for the simultaneous determination of total nitrogen and total phosphorus in freshwater samples using persulphate microwave digestión. Water Res 10:1281–1287CrossRefGoogle Scholar
  35. Jones JI, Sayer CD (2003) Does the fish-invertebrate-periphyton cascade precipitate plant loss in shallow lakes? Ecology 84:2155–2167CrossRefGoogle Scholar
  36. Lamarque P (1990) Electrophysiology of fish in electric fields. In: Cowx IG, Lamarque P (eds) Fishing with electricity-applications in freshwater fisheries management, fishing news books. Blackwell Scientific Publications, Oxford UK, pp 3–33Google Scholar
  37. Larson GL (1976) Social behavior and feeding ability of two phenotypes of Gasterosteus aculeatus in relation to their spatial and trophic segregation in a temperate lake. Can J␣Zool 54:107–121CrossRefGoogle Scholar
  38. Mangnall MJ, Crowe TM (2002) Population dynamics and the physical and financial impacts to cereal crops of the Egyptian Goose Alopochen aegyptiacus on the Agulhas Plain, Western Cape, South Africa. Agric Ecosyst Environ 9:231–246CrossRefGoogle Scholar
  39. Mehner T, Diekmann M, Brämick U, Lemcke R (2005) Composition of fish communities in German lakes as related to lake morphology, trophic state, shore structure and human-use intensity. Freshw Biol 50:70–85CrossRefGoogle Scholar
  40. Meijer ML, De Haan MW, Breukelaar AW, Buiteveld H (1990) Is reduction of the benthivorous fish an important cause of high transparency following biomanipulation in shallow lakes? Hydrobiologia 200–201:303–316CrossRefGoogle Scholar
  41. Michel P, Oberdorff T (1995) Feeding habits of fourteen European freshwater fish species. Cybium 19:5–46Google Scholar
  42. Moss B (2001) The broads. Harper Collins Publishers, LondonGoogle Scholar
  43. Moss B, Carvalho L, Lewes J (2002) The lake at Llandrindod Wells – a restoration comedy? Aquat Conserv: Mar Freshw Ecosyst 12:229–245CrossRefGoogle Scholar
  44. Novotny DW (1990). Electric fishing apparatus and electric fields. In: Cowx IG, Lamarque P (eds) Fishing with electricity-applications in freshwater fisheries management fishing news books. Blackwell Scientific Publications, Oxford, UK, pp 34–88Google Scholar
  45. Perrow MR, Jowitt AJD, Zambrano L (1996a) Sampling fish communities in shallow lowland lakes: point-sample electrofishing versus electrofiishing within stop-nets. Fish Manage Ecol 3:303–313CrossRefGoogle Scholar
  46. Perrow MR, Jowitt AJD, Johnson SR (1996b) Factors affecting the habitat selection of tench in a shallow eutrophic lake. J␣Fish Biol 48:859–870CrossRefGoogle Scholar
  47. Perrow MR, Meijer ML, Dawidowicz P, Coops H (1997) Biomanipulation in shallow lakes: State of the art. Hydrobiologia 342/343:355–365CrossRefGoogle Scholar
  48. Perrow MR, Jowit AJD, Stansfield JH, Phillips GL (1999a) The practical importance of the interactions between fish, zooplankton and macrophytes in shallow lake restoration. Hydrobiologia 395:199–210CrossRefGoogle Scholar
  49. Perrow MR, Jowit AJD, Leigh SAC, Hindes AM, Rhodes JD (1999b) The stability of fish communities in shallow lakes undergoing restoration: expectations and experiences from the Norfolk Broads (U.K.). Hydrobiologia 408/409:85–100CrossRefGoogle Scholar
  50. Persson L (1986) Optimal foraging: the difficulty of exploiting different feeding strategies simultaneously. Oecologia 67:338–341CrossRefGoogle Scholar
  51. Persson L, Diehl S, Johansson L, Andersson G, Hamrin SF (1991) Shifts in fish communities along the productivity gradient of temperate lakes-patterns and the importance of size-structure populations. J Fish Biol 38:281–293CrossRefGoogle Scholar
  52. Persson L, Crowder LB (1998) Fish-habitat interactions mediated via ontogenetic niche shifts. In: Jeppesen E, Søndergaard Ma, Søndergaard Mo, Christoffersen K (eds) The structuring role of submerged macrophytes in lakes. Ecological Studies Series Springer Verlag, New York, pp 3–23Google Scholar
  53. Proman JM, Reynolds JD (2000). Differences in head shape of the European eel, Anguilla anguilla (L.). Fish Manage Ecol 7:349–354Google Scholar
  54. Roberts J, Chick A, Oswald L, Thompson P (1995) Effects of carp Cyprinus carpio L. an exotic benthivorous fish, on aquatic plants and water quality in experimental ponds. Mar Freshw Res 46:1171–1180CrossRefGoogle Scholar
  55. Scheffer M (1998) Ecology of shallow lakes. Chapman & Hall, LondonGoogle Scholar
  56. Scheffer M, de Boer RJ (1995) Implications of spatial heterogeneity for the paradox of enrichment. Ecology 76:2270–2277CrossRefGoogle Scholar
  57. Scheffer M, Carpenter SR, Foley JA, Folke C, Walker B (2001) Catastrophic shifts in ecosystems. Nature 413:591–596PubMedCrossRefGoogle Scholar
  58. Scheffer M, Hosper SH, Meijer M-L, Moss B, Jeppesen E (1993) Alternative equilibria in shallow lakes. Trends Ecol Evol 8:275–279CrossRefGoogle Scholar
  59. Scheffer M, Portielje R, Zambrano L (2003) Fish facilitate wave resuspension of sediments. Limnol Oceanogr 48:1920–1926CrossRefGoogle Scholar
  60. Schriver P, Bøgestrand J, Jeppesen E, Søndergaard M (1995) Impact of submerged macrophytes on fish-zooplankton-phytoplankton interactions: large-scale enclosure experiments in a shallow lake. Freshw Biol 33:255–270CrossRefGoogle Scholar
  61. Scott WB, Crossman EJ (1973) Freshwater fishes of Canada. Bull Fish Res Board Canada 184:1–966Google Scholar
  62. Skov C, Berg S (1999) Utilization of natural and artificial habitats by pike in a biomanipulated lake. Hydrobiologia 408/409:115–122CrossRefGoogle Scholar
  63. Skov C, Perrow MR, Berg S, Skovgaard H (2002) Changes in the fish community and water quality during seven years of stocking piscivorous fish in a shallow lake. Freshw Biol 47:2388–2400CrossRefGoogle Scholar
  64. Skov C, Lousdal O, Johansen PH, Berg S (2003) Piscivory of␣0+ pike (Esox lucius L.) in a small eutrophic lake and␣its implication for biomanipulation. Hydrobiologia 506–509:481–487CrossRefGoogle Scholar
  65. Smith P (2001) Can fish determine the conservation value of shallow lakes in the UK? Br Wildlife 13:10–15Google Scholar
  66. Søndergaard M, Jeppesen E, Jensen JP, Amsinck SL (2005a) Water Framework Directive: ecological classification of Danish lakes. J Appl Ecol 42:616–629CrossRefGoogle Scholar
  67. Søndergaard M, Jeppesen E, Jensen JP (2005b) Pond or lake: does it make any difference? Archiv für Hydrobiologie 162:143–165CrossRefGoogle Scholar
  68. Spanovskaya VD, Grygorash VA (1977) Development and food of age-0 eurasian perch (Perca fluviatilis) in reservoirs near Moscow, USSR. J Fish Res Board Canada 34:1551–1558Google Scholar
  69. Stansfield JH, Perrow MR, Tench LD, Jowitt AJD, Taylor AAL (1997) Submerged macrophytes as refuges for grazing Cladocera against fish predation: observations on seasonal changes in relation to macrophyte cover and predation pressure. Hydrobiologia 342/343:229–240CrossRefGoogle Scholar
  70. Svanbäck R, Persson L (2004) Individual diet specialization, niche width and population dynamics: implications for trophic polymorphisms. J Animal Ecol 73:973–982CrossRefGoogle Scholar
  71. Talling JF, Driver D (1961) Some problems in the estimation of chlorophyll a in phytoplankton. In: Doty MS (ed) Primary Production Measurement Marine Freshwater, University of Hawaii. US. Energy Commission Publ. TID 7633:Google Scholar
  72. van Densen WLT (1994) Predator enhancement in freshwater fish communities. In: Cowx IG (ed) Rehabilitation of freshwater fisheries, fishing news books. Blackwell Scientific Publications, Oxford UK, pp 102–119Google Scholar
  73. Vasek M, Kubecka J (2004) In situ diel patterns of zooplankton consumption by subadult/adult roach Rutilus rutilus, bream Abramis brama, and bleak Alburnus alburnus. Folia Zoologica 53:203–214Google Scholar
  74. Wetzel RG, GE Likens (1991) Limnological Analysis. Springer-Verlag, New York, 391Google Scholar
  75. Williams A, Moss B (2003) Effects on different fish species and biomass on plankton interactions in a shallow lake. Hydrobiologia 491:331–346CrossRefGoogle Scholar
  76. Zambrano L, Hinojosa D (1999) Direct and indirect effects of carp (Cyprinus carpio L.) on macrophyte and benthic communities in experimental shallow ponds in central México. Hydrobiologia 409:131–138CrossRefGoogle Scholar
  77. Zambrano L, Perrow MR, Macias-Garcia C, Aguirre-Hidalgo V (1999) Impact of introduced carp (Cyprinus carpio) in subtropical shallow ponds in central México. J Aquat Ecosyst Stress Recovery 6:281–288CrossRefGoogle Scholar
  78. Zambrano L, Scheffer M, Martínez-Rámos M (2001) Catastrophic response of lakes to benthivorous fish introduction. Oikos 94:344–350CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Luis Zambrano
    • 1
    Email author
  • Martin R. Perrow
    • 2
  • Carl D. Sayer
    • 3
  • Mark L. Tomlinson
    • 2
  • Thomas A. Davidson
    • 3
  1. 1.Instituto de BiologíaUNAMMéxicoMéxico
  2. 2.ECON Ecological ConsultancyNorwich Research ParkNorwichUK
  3. 3.Environmental Change Research Centre, Department of GeographyUniversity College LondonLondonUK

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