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Marine Biology

, Volume 160, Issue 2, pp 465–478 | Cite as

Functional responses of juvenile herring and sprat in relation to different prey types

  • R. BrachvogelEmail author
  • L. Meskendahl
  • J.-P. Herrmann
  • A. Temming
Original Paper

Abstract

The relationship between particulate-feeding rates and prey concentrations (functional response) of juvenile herring and sprat (5–9 cm total length) was investigated in controlled feeding experiments monitored by an underwater camera system. A special tank system was developed allowing the regulation and quantification of low prey concentrations (1–160 L−1). Non-evasive Artemia nauplii was used as prey to estimate the maximum biting rate of both predators. In contrast, Acartia tonsa with a high escape ability was used as a realistic prey type. Herring and sprat showed a type II functional response for both prey types. Nonlinear mixed effects model revealed no significant difference between the functional responses of both predators, except that herring showed significantly higher biting rates than sprat at A. tonsa concentrations below ~40 L−1. For both predators feeding rates were significantly higher with Artemia nauplii than with A. tonsa. Video analysis indicated that sprat, unlike herring, is an obligate particulate-feeder.

Keywords

Functional Response Prey Item Prey Type Handling Time Akaike Information Criterion 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors gratefully acknowledge the help of J. Lütke and S. Stäcker in catching fish and maintaining them in the aquarium. Furthermore, we like to thank all trainees in helping to perform the experiments. Our thanks also go to two anonymous referees provided helpful comments that improved the manuscript. Funding of this study was provided in part by the VECTORS (VECTORS of Change in Oceans and Seas Marine Life, Impact on Economic Sectors) Project.

References

  1. Aggrey SE (2008) Logistic nonlinear mixed effects model for estimating growth parameters. Poult Sci 88:276–280CrossRefGoogle Scholar
  2. Alshuth S (1989) Variation in growth of adult North Sea sprat (Sprattus sprattus L.). ICES CM 1989/H: 14Google Scholar
  3. Arrhenius F (1996) Diet composition and food selectivity of 0-group herring (Clupea harengus L.) and sprat (Sprattus sprattus (L.)) in the northern Baltic Sea. ICES J Mar Sci 53:701–712Google Scholar
  4. Arrhenius F, Hasson S (1993) Food consumption of larval, young and adult herring and sprat in the Baltic Sea. Mar Ecol Prog Ser 96:125–137CrossRefGoogle Scholar
  5. Batty RS, Blaxter JHS, Libby DA (1986) Herring (Clupea harengus) filter-feeding in the dark. Mar Biol 91:371–375CrossRefGoogle Scholar
  6. Batty RS, Blaxter JHS, Richard JM (1990) Light intensity and the feeding behaviour of herring, Clupea harengus. Mar Biol 107:383–388CrossRefGoogle Scholar
  7. Bernreuther M (2007) Investigations on the feeding ecology of Baltic Sea herring (Clupea harengus L.) and sprat (Sprattus sprattus L.). Dissertation, University of HamburgGoogle Scholar
  8. Bernreuther M, Herrmann J-P, Temming A (2008) Laboratory experiments on the gastric evacuation of juvenile herring. J Exp Mar Biol Ecol 363:1–11CrossRefGoogle Scholar
  9. Blaxter JHS, Jones MP (1967) The development of the retina and retinomotor responses in the herring. J Mar Biol Assoc UK 47:677–697CrossRefGoogle Scholar
  10. Broekhuizen N, McKenzie E (1995) Patterns of abundance for Calanus and smaller copepods in the North Sea: time series decomposition of two CPR data sets. Mar Ecol Prog Ser 118:103–120CrossRefGoogle Scholar
  11. Buskey EJ (1994) Factors affecting feeding selectivity of visual predators on the copepod Acartia tonsa: locomotion, visibility and escape responses. Hydrobiologia 292(293):447–453CrossRefGoogle Scholar
  12. Buskey EJ, Coulter C, Strom S (1993) Locomotory pattern of microzooplankton: potential effects on food selectivity of larval fish. Bull Mar Sci 53:29–43Google Scholar
  13. Casini M, Cardinale M, Arrhenius F (2004) Feeding preferences of herring (Clupea harengus) and sprat (Sprattus sprattus) in the southern Baltic Sea. ICES J Mar Sci 61:1267–1277CrossRefGoogle Scholar
  14. Casini M, Lovgren J, Hjelm J, Cardinale M, Molinero J-C, Kornilovs G (2008) Multi-level trophic cascades in a heavily exploited open marine ecosystem. Proc R Soc B 275:1793–1801CrossRefGoogle Scholar
  15. Colebrook JM (1979) Continuous plankton records: seasonal cycle of phytoplankton and copepods in the North Atlantic Ocean and the North Sea. Mar Biol 51:23–32CrossRefGoogle Scholar
  16. Crowder LB (1985) Optimal foraging and feeding mode shift in fishes. Environ Biol Fishes 12(1):57–62CrossRefGoogle Scholar
  17. Cury P, Bakun A, Crawford RJM, Jarre A, Quinones RA, Shannon LJ, Verheye HM (2000) Small pelagics in upwelling systems: patters of interaction and structural changes in “wasp-waist” ecosystem. ICES J Mar Sci 57(3):603–618CrossRefGoogle Scholar
  18. De Silva SS (1973) Food and feeding habits of the herring Clupea harengus and the sprat C. sprattus in inshore waters of the west coast of Scotland. Mar Biol 20:282–290CrossRefGoogle Scholar
  19. Durbin AG (1979) Food selection by plankton feeding fishes. In: Stroud RH, Clepper H (eds) Predator-prey systems in fisheries management. Sport Fishing Institute, Washington, DC, pp 203–218Google Scholar
  20. Folt CL, Burns CW (1999) Biological drivers of zooplankton patchiness. Trends Ecol Evol 14:300–305CrossRefGoogle Scholar
  21. Fulton EA, Fuller M, Smith ADM, Punt AE (2004) Ecological indicators of the ecosystem effects of fishing: final report. Australian Fisheries Management Authority Report R/1546Google Scholar
  22. Gibson RN, Ezzi IA (1985) Effect of particle concentration on filter- and particulate-feeding in the herring Clupea harengus. Mar Biol 88:109–116CrossRefGoogle Scholar
  23. Gibson RN, Ezzi IA (1990) Relative importance of prey size and concentration in determining the feeding behaviour of the herring Clupea harengus. Mar Biol 107:357–362CrossRefGoogle Scholar
  24. Gibson RN, Ezzi IA (1992) The relative profitability of particulate- and filter-feeding in herring, Clupea harengus L. J Fish Biol 40:577–590CrossRefGoogle Scholar
  25. Hairstone NG, Li KT, Easter SS (1982) Fish vision and the detection of planktonic prey. Science 218(4578):1240–1242CrossRefGoogle Scholar
  26. Hawkins A, Knudsen FR, Davenport J, McAllen R, Bloomfield HJ, Schilt C, Johnson P (2012) Grazing by sprat schools upon zooplankton within an enclosed marine lake. J Exp Mar Biol Ecol 411:59–65CrossRefGoogle Scholar
  27. Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398CrossRefGoogle Scholar
  28. Holling CS (1966) The functional response of invertebrate predators to prey density. Mem Entomol Soc Can 48:1–86CrossRefGoogle Scholar
  29. Holste L, Peck MA (2006) The effects of temperature and salinity on eggs production and hatching success of Baltic Acartia tonsa (Copepoda: Calanoida): a laboratory investigation. Mar Biol 148:1061–1070CrossRefGoogle Scholar
  30. Hunter JR (1972) Swimming and feeding behavior of larval anchovy Engraulis mordax. Fish Bull 70(3):821–838Google Scholar
  31. James AG, Findlay KP (1989) Effect of particle size and concentration on the feeding behaviour, selectivity and rates of food ingestion by the Cape anchovy Engraulis capensis. Mar Ecol Prog Ser 50:275–294CrossRefGoogle Scholar
  32. Janssen J (1976) Feeding modes and prey size selection in the alewife (Alosa pseudoharengus). J Fish Res Board Can 33(9):1972–1975CrossRefGoogle Scholar
  33. Jeschke JM, Kopp M, Tollrian R (2002) Predator functional responses: discriminating between handling and digesting prey. Ecol Monogr 72(1):95–112CrossRefGoogle Scholar
  34. Jeschke JM, Kopp M, Tollrian R (2004) Consumer-food systems: why type I functional responses are exclusive to filter feeders. Biol Rev 79:337–349CrossRefGoogle Scholar
  35. Juliano SA (2001) Nonlinear curve fitting. In: Scheiner SM, Gurevitch J (eds) Design an analysis of ecological experiments. Oxford University Press, New York, pp 178–196Google Scholar
  36. Kils U (1992) The ecoSCOPE and dynIMAGE: microscale tools for in situ studies of predator-prey interaction. Arch Hydrobiol Beih 36:83–96Google Scholar
  37. Kiørboe T, Andersen A, Langlois VJ, Jakobsen HH (2010) Unsteady motion: escape jumps in planktonic copepods, their kinematics and energetics. J R Soc Interface 7:1591–1602CrossRefGoogle Scholar
  38. Köster FW, Möllmann C, Neuenfeldt S, Vinther M, St. John MA, Tomkiewicz L, Voss R, Hinrichsen H-H, MacKenzie B, Kraus G, Schnack D (2003) Fish stock development in the central Baltic Sea (1974–1999) in relation to variability in the environment. ICES Mar Sci Symp 219:294–306Google Scholar
  39. Last JM (1989) The food of herring, Clupea harengus, in the North Sea, 1983–1986. J Fish Biol 34(4):489–501CrossRefGoogle Scholar
  40. Lazzaro X (1987) A review of planktivorous fishes: their evolution, feeding behaviours, selectivities, and impacts. Hydrobiologia 146:97–167CrossRefGoogle Scholar
  41. Leong RJH, O’Connell CP (1969) A laboratory study of particulate and filter feeding of the Northern anchovy (Engraulis mordax). J Fish Res Board Can 26:557–582CrossRefGoogle Scholar
  42. Lindstrom MJ, Bates DM (1990) Nonlinear mixed effects models for repeated measures data. Biometrics 46(3):673–687CrossRefGoogle Scholar
  43. Maes J, Ollevier F (2002) Size structure and feeding dynamics in estuarine clupeoid fish schools: field evidence for the school trap hypothesis. Aquat Living Resour 15:211–216CrossRefGoogle Scholar
  44. Maes J, Tackx M, Soetaert K (2005) The predation impact of juvenile herring Clupea harengus and sprat Sprattus sprattus on estuarine zooplankton. Hydrobiologia 540:225–235CrossRefGoogle Scholar
  45. Megrey BA, Rose KA, Klumb RA, Hay DE, Werner FE, Eslinger DL, Smith SL (2007) A bioenergetics-based population dynamics model of Pacific herring (Clupea harengus pallasi) coupled to a lower trophic level nutrient-phytoplankton-zooplankton model: description, calibration, and sensitivity analysis. Ecol Model 202:144–164CrossRefGoogle Scholar
  46. Möllmann C, Kornilovs G, Fetter M, Köster FW (2004) Feeding ecology of central Baltic Sea herring and sprat. J Fish Biol 65(6):1563–1581CrossRefGoogle Scholar
  47. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-Plus. Springer, New YorkCrossRefGoogle Scholar
  48. Pinheiro JC, Bates DM, DebRoy S, Sarkar D, R Development Core Team (2011) nlme: Linear and nonlinear mixed effects models, pp 1–102 (R package version 3)Google Scholar
  49. R Development Core Team (2011) R: a language and environment for statistical computing, reference index version 2.13.1. R Foundation for Statistical Computing, Vienna, Austria (ISBN 3-900051-07-0, http://www.R-project.org)
  50. Rosenthal H (1969) Untersuchungen über das Beutefangverhalten bei Larven des Herings Clupea harengus. Mar Biol 3:208–221CrossRefGoogle Scholar
  51. Rudstam LG, Aneer G, Hildén M (1994) Top-down control in the pelagic Baltic ecosystem. Dana 10:105–129Google Scholar
  52. Sarnelle O, Wilson AE (2008) Type III functional response in Daphnia. Ecology 89(6):1723–1732CrossRefGoogle Scholar
  53. Shin Y-J, Travers M, Maury O (2010) Coupling low and high trophic level models: towards a pathways-orientated for end-to-end models. Prog Oceanogr 84(1–2):105–112CrossRefGoogle Scholar
  54. Singarajah KV (1969) Escape reaction of zooplankton: the avoidance of a pursuing siphon tube. J Exp Mar Biol Ecol 3:171–178CrossRefGoogle Scholar
  55. Soetaert K, Van Rijswijk P (1993) Spatial and temporal patterns of the zooplankton in the Westerschelde estuary. Mar Ecol Prog Ser 97:47–59CrossRefGoogle Scholar
  56. Stockwell JD, Johnson BM (1997) Refinement and calibration of a bioenergetics-based model for kokanee (Oncorhynchus nerka). Can J Fish Aquat Sci 54:2659–2676Google Scholar
  57. Stockwell JD, Johnson BM (1999) Field evaluation of a bioenergetics-based foraging model for kokanee (Oncorhynchus nerka). Can J Fish Aquat Sci 56:140–151CrossRefGoogle Scholar
  58. Strickler JR, Udvadia AJ, Marino J, Radabaugh N, Zairek J, Nihongi A (2005) Visibility as a factor in the copepod-planktivorous fish relationship. Sci Mar 69(1):111–124Google Scholar
  59. Trager G, Achituv Y, Genin A (1994) Effects of prey escape ability, flow speed, and predator feeding mode on zooplankton capture by barnacles. Mar Biol 120:251–259CrossRefGoogle Scholar
  60. van der Lingen CD (1994) Effect of particle size and concentration on the feeding behaviour of adult pilchard Sardinops sagax. Mar Ecol Prog Ser 109:1–13CrossRefGoogle Scholar
  61. Varpe Ø, Fiksen Ø (2010) Seasonal plankton-fish interactions: light regime, prey phenology, and herring foraging. Ecology 91(2):311–318CrossRefGoogle Scholar
  62. Viitasalo M, Flinkman J, Viherluoto M (2001) Zooplanktivory in the Baltic Sea: a comparison of prey selectivity by Clupea harengus and Mysis mixta, with reference to prey escape reactions. Mar Ecol Prog Ser 216:191–200CrossRefGoogle Scholar
  63. Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R, 1st edn. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • R. Brachvogel
    • 1
    Email author
  • L. Meskendahl
    • 1
  • J.-P. Herrmann
    • 1
  • A. Temming
    • 1
  1. 1.Institute for Hydrobiology and Fisheries ScienceUniversity of HamburgHamburgGermany

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