Skip to main content
Log in

Angling baits and invasive crayfish as important trophic subsidies for a large cyprinid fish

  • Research Article
  • Published:
Aquatic Sciences Aims and scope Submit manuscript

Abstract

Invasive species and anthropogenic sources of allochthonous trophic subsidies can have substantial ecological consequences for freshwater ecosystems, including modifying the diet of consumers and altering food web structure. Here, the diet of an omnivorous cyprinid fish, European barbel Barbus barbus, was assessed in relation to the presence of invasive signal crayfish Pacifastacus leniusculus and pelletized fish-meal in four rivers in England. Pellets are often used in large quantities by river anglers and thus could provide an important trophic subsidy, not only to the fish but also indirectly via P. leniusculus. Carbon and nitrogen stable isotopes were used to estimate the proportion of diet assimilated from natural sources and from P. leniusculus and pellets by B. barbus of lengths between 420 and 800 mm. Pellets generally made a large contribution to the overall biomass of B. barbus (up to 59 % of population diet) and in the two rivers where they were present, P. leniusculus were also an important resource (up to 30 % of population diet). The proportion derived from macro-invertebrates (excluding P. leniusculus) was substantially lower. Stable isotope mixing models further demonstrated considerable intraspecific variability in B. barbus diet within the rivers, with pellets comprising up to 79 % of the biomass of individual B. barbus in rivers where P. leniusculus was absent. Where present, P. leniusculus effectively replaced and thus reduced the contribution of pellets to individual fish diet. Thus, isotopic evidence from three of the four rivers indicates that B. barbus populations are heavily reliant (>50 %) upon angler-introduced baits that act as an important allochthonous subsidy and will also prey upon invasive P. leniusculus where they are present.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Arlinghaus R, Niesar N (2005) Nutrient digestibility of angling baits for carp, Cyprinus carpio, with implications for groundbait formulation and eutrophication control. Fish Man Ecol 12:91–97

    Article  Google Scholar 

  • Baras E (1995a) Seasonal activities of Barbus barbus L.: effect of temperature on time-budgeting. J Fish Biol 46:816–828

    Google Scholar 

  • Baras E (1995b) Thermal related variations of seasonal and daily spawning periodicity in Barbus barbus. J Fish Biol 46:915–917

    Google Scholar 

  • Beja PR (1996) An analysis of otter Lutra lutra predation on introduced American crayfish Procambarus clarkii in Iberian streams. J Appl Ecol 33:1156–1170

    Article  Google Scholar 

  • Blake MA, Hart PJB (1995) The vulnerability of juvenile signal crayfish to perch and eel predation. Freshw Biol 33:233–244

    Article  Google Scholar 

  • Bobeldyk AM, Lamberti GA (2010) Stream food web responses to a large omnivorous invader, Orconectes rusticus (Decapoda, Cambaridae). Crustaceana 83:641–657. doi:10.1163/001121610X49103

    Article  Google Scholar 

  • Britton JR, Pegg J (2011) Ecology of European Barbel Barbus barbus: implications for river, fishery, and conservation management. Rev Fish Sci 19:321–330. doi:10.1080/10641262.2011.599886

    Article  Google Scholar 

  • Britton JR, Davies GD, Harrod C (2010) Trophic interactions and consequent impacts of the invasive fish Pseudorasbora parva in a native aquatic foodweb: a field investigation in the UK. Biol Invasions 12:1533–1542. doi:10.1007/s10530-009-9566-5

    Article  Google Scholar 

  • Britton JR, Pegg J, Davies GD (2012) Spatial variation in the somatic growth of European barbel Barbus barbus: a UK perspective. Ecol Freshw Fish 22:21–29

    Article  Google Scholar 

  • Cherghou S, Khodari M, Yaâkoubi F, Benabid M, Badri A (2002) Contribution to study a barbel (Barbus barbus callensis Valenciennes, 1842) diet in Morrocain Medium-Atlas stream: oued Boufekrane. Revue des Sci de l’Eau 15:153–163

    Google Scholar 

  • Correia AM (2001) Seasonal and interspecific evaluation of predation by mammals and bird on the introduced red swamp crayfish Procambarus clarkii (Crustacea, Cambaridae) in a freshwater marsh (Portugal). J Zool 255:533–541

    Article  Google Scholar 

  • Corse E, Costedoat C, Chappaz R, Pech N, Martin JF, Gilles A (2010) A PCR-based method for diet analysis in freshwater organisms using 18S rDNA barcoding on faeces. Mol Ecol Res 10:96–108. doi:10.1111/j.1755-0998.2009.02795.x

    Article  CAS  Google Scholar 

  • Coulas RA, Macisaac HJ, Dunlop W (1998) Selective predation on an introduced zooplankter (Bythotrephes cederstroemi) by lake herring (Coregonus artedii) in Harp Lake, Ontario. Freshw Biol 40:343–355

    Article  Google Scholar 

  • Demétrio JA, Gomes LC, Latini JD, Agostinho AA (2012) Influence of net cage farming on the diet of associated wild fish in a Neotropical reservoir. Aquaculture 330–333:172–178. doi:10.1016/j.aquaculture.2011.11.026

    Article  Google Scholar 

  • Ellis BK, Stanford JA, Goodman D, Stafford CP, Gustafson DL, Beauchamp DA, Chess DW, Craft JA, Deleray MA, Hansen BS (2011) Long-term effects of a trophic cascade in a large lake ecosystem. Proc Natl Acad Sci USA 108:1070–1075

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fernandez-Jover D, Arechavala-Lopez P, Martinez-Rubio L, Tocher DR, Bayle-Sempere JT, Lopez-Jimenez JA, Martinez-Lopez FJ, Sanchez-Jerez P (2011a) Monitoring the influence of marine aquaculture on wild fish communities: benefits and limitations of fatty acid profiles. Aquac Environ Interact 2:39–47. doi:10.3354/aei00029

    Article  Google Scholar 

  • Fernandez-Jover D, Martinez-Rubio L, Sanchez-Jerez P, Bayle-Sempere JT, Lopez Jimenez JA, Martínez Lopez FJ, Bjørn PA, Uglem I, Dempster T (2011b) Waste feed from coastal fish farms: a trophic subsidy with compositional side-effects for wild gadoids. Estuar Coast Shelf S 91:559–568. doi:10.1016/j.ecss.2010.12.009

    Article  CAS  Google Scholar 

  • Garvey JE, Rettig JE, Stein RA, Lodge DM, Klosiewski SP (2003) Scale-dependent associations among fish Predation, littoral habitat, and distributions of crayfish species. Ecology 84:3339–3348

    Article  Google Scholar 

  • Grey J (2006) The use of stable isotope analyses in freshwater ecology: current awareness. Pol J Ecol 54:563–584

    CAS  Google Scholar 

  • Grey J, Waldron S, Hutchinson R (2004) The utility of carbon and nitrogen isotope analyses to trace contributions from fish farms to the receiving communities of freshwater lakes: a pilot study in Esthwaite Water, UK. Hydrobiologia 524:253–262

    Article  Google Scholar 

  • Grey J, Graham CT, Britton JR, Harrod C (2009) Stable isotope analysis of archived roach (Rutilus rutilus) scales for retrospective study of shallow lake responses to nutrient reduction. Freshw Biol 54:1663–1670. doi:10.1111/j.1365-2427.2009.02215.x

    Article  CAS  Google Scholar 

  • Guan RZ, Wiles PR (1997) Ecological impact of introduced crayfish on benthic fishes in a British lowland river. Conserv Biol 11:641–647

    Article  Google Scholar 

  • Harmon JP, Ives AR, Moran NA (2009) Species response to environmental change: impacts of food web interactions and evolution. Science 323:1347–1350. doi:10.1126/science.1167396

    Article  CAS  PubMed  Google Scholar 

  • Hein CL, Roth BM, Ives AR, Vander Zanden MJ (2006) Fish predation and trapping for rusty crayfish (Orconectes rusticus) control: a whole-lake experiment. Can J Fish Aquat Sci 63:383–393. doi:10.1139/F05-229

    Article  Google Scholar 

  • Hutchinson JJ, Trueman CN (2006) Stable isotope analyses of collagen in fish scales: limitations set by scale architecture. J Fish Biol 69:1874–1880. doi:10.1111/j.1095-8649.2006.01234.x

    Article  CAS  Google Scholar 

  • Jackson MC, Grey J (2013) Accelerating rates of freshwater invasions in the catchment of the River Thames. Biol Invasions 15:945–951. doi:10.1007/s10530-012-0343-5

    Article  Google Scholar 

  • Jackson MC, Donohue I, Jackson AL, Britton JR, Harper DM, Grey J (2012) Population-level metrics of trophic structure based on stable isotopes and their application to invasion ecology. PLoS ONE 7:e31757. doi:10.1371/journal.pone.0031757

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jackson MC, Allen R, Pegg J, Britton JR (2013) Do trophic subsidies affect the outcome of introductions of a non-native freshwater fish? Freshw Biol 58:2144–2153. doi:10.1111/fwb.12197

    Article  Google Scholar 

  • Jackson MC, Jones T, Milligan M, Sheath D, Taylor J, Ellis A, England J, Grey J (2014) Niche differentiation among invasive crayfish and their impacts on ecosystem structure and functioning. Freshw Biol 59:1123–1135. doi:10.1111/fwb.12333

    Article  Google Scholar 

  • Jefferies RL (2000) Allochthonous inputs: integrating population changes and food-web dynamics. Trend Ecol Evol 15:19–22

    Article  Google Scholar 

  • Jones RI, Grey J, Sleep D, Quarmby C (1998) An assessment, using stable isotopes, of the importance of allochthonous organic carbon sources to the pelagic food web in loch ness. Proc R Soc Lond B 265:105–110. doi:10.1098/rspb.1998.0270

    Article  Google Scholar 

  • Kottelat M, Freyhof J (2007) Handbook of European freshwater fishes. Kottelat, Cornol

    Google Scholar 

  • Kouba A, Petrusek A, Kozák P (2014) Continental-wide distribution of crayfish species in Europe: update and maps. Knowl Manag Aquat Ecosyst 413:05

    Article  Google Scholar 

  • Lewin WC, Arlinghaus R, Mehner T (2006) Documented and potential biological impacts of recreational fishing: insights for management and conservation. Rev Fish Sci 14:305–367. doi:10.1080/10641260600886455

    Article  Google Scholar 

  • MacDougall AS, Turkington R (2005) Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86:42–55

    Article  Google Scholar 

  • Marcarelli AM, Baxter CV, Mineau MM, Hall RO (2011) Quantity and quality: unifying food web and ecosystem perspectives on the role of resource subsidies in freshwaters. Ecology 92:1215–1225

    Article  PubMed  Google Scholar 

  • Marczak LB, Richardson JS, Thompson RM (2007) Meta-analysis: trophic level, habitat, and productivity shape the food web effects of resource subsidies. Ecology 88:140–148

    Article  PubMed  Google Scholar 

  • McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390. doi:10.1034/j.1600-0706.2003.12098.x

    Article  CAS  Google Scholar 

  • Naylor RL, Goldburg RJ, Primavera JH, Kautsky N, Beveridge MCM, Clay J, Folke C, Lubchenco J, Mooney H, Troell M (2000) Effect of aquaculture on world fish supplies. Nature 405:1017–1024. doi:10.1038/35016500

    Article  CAS  PubMed  Google Scholar 

  • Niesar M, Arlinghaus R, Rennert B, Mehner T (2004) Coupling insights from a carp, Cyprinus carpio, angler survey with feeding experiments to evaluate composition, quality and phosphorus input of groundbait in coarse fishing. Fish Man Ecol 11:225–235

    Article  Google Scholar 

  • Nyström P, Stenroth P, Holmoqvist N, Berglund O, Larsson P, Granéli W (2006) Crayfish in lakes and streams: individual and population responses to predation, productivity and substratum availability. Freshw Biol 51:2096–2113. doi:10.1111/j.1365-2427.2006.01641.x

    Article  Google Scholar 

  • Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5(3):e9672. doi:10.1371/journal.pone.0009672

    Article  PubMed Central  PubMed  Google Scholar 

  • Pegg J, Britton JR (2011) Effects of inter- and intra-specific competition on the growth rates of juvenile European barbel Barbus barbus used in the stock enhancement of UK fisheries. Fish Res 112:8–12. doi:10.1016/j.fishres.2011.08.003

    Article  Google Scholar 

  • Perga ME, Gerdeaux D (2005) Are fish what they eat all year round? Oecologia 144:598–606

    Article  CAS  PubMed  Google Scholar 

  • Petchey OL, McPhearson PT, Casey TM, Morin PJ (1999) Environmental warming alters food-web structure and ecosystem function. Nature 402:69–72. doi:10.1038/47023

    Article  CAS  Google Scholar 

  • Phillips DL, Newsome SD, Gregg JW (2005) Combining sources in stable isotope mixing models: alternative methods. Oecologia 144:520–527. doi:10.1007/s00442-004-1816-8

    Article  PubMed  Google Scholar 

  • Pinnegar JK, Polunin NVC (1999) Differential fractionation of δ 13C and δ 15N among fish tissues: implications for the study of trophic interactions. Func Ecol 13:225–231

    Article  Google Scholar 

  • Piria M, Treer T, Aničić I, Safner R, Odak T (2005) The natural diet of five cyprinid fish species. Agric Conspec Sci 70:21–28

    Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718

    Article  Google Scholar 

  • R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org/

  • Sato T, Watanabe K (2013) Do stage-specific functional responses of consumers dampen the effects of subsidies on trophic cascades in streams? J Anim Ecol. doi:10.1111/1365-2656.12192

    PubMed  Google Scholar 

  • Tablado Z, Tella JL, Sánchez-Zapata JA, Hiraldo F (2010) The paradox of the long-term positive effects of a North American crayfish on a European community of predators. Conserv Biol 24:1230–1238

    Article  PubMed  Google Scholar 

  • Tacon AGJ, Metian M (2008) Global overview on the use of fish meal and fish oil in industrially compounded aquafeeds: trends and future prospects. Aquaculture 285:146–158. doi:10.1016/j.aquaculture.2008.08.015

    Article  CAS  Google Scholar 

  • Thomas CL, Taylor CA (2013) Scavenger or predator? Examining a potential predator–prey relationship between crayfish and benthic fish in stream food webs. Freshw Sci 32:1309–1317. doi:10.1899/12-169.1

    Article  Google Scholar 

  • Vander Zanden MJ, Rasmussen JB, Casselman JM (1999) Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401:464–467

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the Barbel Society for their support in the completion of the work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. Robert Britton.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bašić, T., Britton, J.R., Jackson, M.C. et al. Angling baits and invasive crayfish as important trophic subsidies for a large cyprinid fish. Aquat Sci 77, 153–160 (2015). https://doi.org/10.1007/s00027-014-0370-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00027-014-0370-7

Keywords

Navigation