Too short to spawn? Implications of small body size and swimming distance on successful migration and maturation of the European eel Anguilla anguilla

Journal of Fish Biology

Volumn 78, Issue 4, 2011, Pages 1073-1089

  Clevestam, P D ^a   Ogonowski, M ^b   Sjoberg N B ^a   Wickstrom H ^a  

^a INSTITUTE OF FRESHWATER RESEARCH   (Sweden)

^b STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Anguillicoloides crassus; Cost of transport; Fat content; Reproduction; Spawning

Indexed keywords

ADIPOSE TISSUE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BODY SIZE; EEL; FEMALE; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; METABOLISM; PHYSIOLOGY; POPULATION MIGRATION; SWIMMING;

ADIPOSE TISSUE; ANIMAL MIGRATION; ANIMALS; BODY SIZE; EELS; FEMALE; MODELS, BIOLOGICAL; SWIMMING;

ANGUILLA ANGUILLA;

EID: 79953297270     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2011.02920.x     Document Type: Article

References (66)

1. Aarestrup, K., Okland, F., Hansen, M. M., Righton, D., Gargan, P., Castonguay, M., Bernatchez, L., Howey, P., Sparholt, H., Pedersen, M. I. & McKinley, R. S. (2009). Oceanic spawning migration of the European eel (Anguilla anguilla). Science 325, 1660.
2. Belpaire, C. G. J., Goemans, G., Geeraerts, C., Quataert, P., Parmentier, K., Hagel, P. & De Boer, J. (2009). Decreasing eel stocks: survival of the fattest? Ecology of Freshwater Fish 18, 197-214.
3. Beregi, A., Molnar, K., Bekesi, L. & Szekely, C. (1998). Radiodiagnostic method for studying swimbladder inflammation caused by Anguillicola crassus (Nematoda: Dracunculoidea). Diseases of Aquatic Organisms 34, 155-160.
4. Bergersen, R. & Klemetsen, A. (1988). Freshwater eel Anguilla anguilla (L.) from north Norway, with emphasis on occurrence, food, age, and downstream migration. Nordic Journal of Freshwater Research 64, 54-66.
5. Berntsson, K. E. (1971). An account of some aspects of the fishery for eels in Sweden. EIFAC Technical Paper 14, 105-112.
6. Bertin, L. (1956). Eels, a Biological Study. London: Cleaver-Hume.
7. Boëtius, I. & Boëtius, J. (1980). Experimental naturation of female silver eels, Anguilla anguilla. Estimates of fecundity and energy reserves for migration and spawning. Dana-a Journal of Fisheries and Marine Research 1, 1-28.
8. Boëtius, I. & Boëtius, J. (1985). Lipid and protein content in Anguilla anguilla during growth and starvation. Dana-a Journal of Fisheries and Marine Research 4, 1-17.
9. Boon, J. H., Cannaerts, V. M. H., Augustijn, H., Machiels, M. A. M., De Charleroy, D. & Ollevier, F. (1990). The effect of different infection levels with infective larvae of Anguillicola crassus on haematological parameters of European eel (Anguilla anguilla). Aquaculture 87, 243-253.
10. Brett, J. R. (1964). The respiratory metabolism and swimming performance of young sockeye salmon. Journal of the Fisheries Research Board of Canada 21, 1183-1226.
11. Brett, J. R. (1965). The relation of size to the rate of oxygen consumption and sustained swimming speeds of sockeye salmon (Oncorhynchus nerka). Journal of the Fisheries Research Board of Canada 22, 1491.
12. Brett, J. R. & Glass, N. R. (1973). Metabolic rates and critical swimming speeds of sockeye salmon (Oncorhynchus nerka) in relation size and temperature. Journal of the Fisheries Research Board of Canada 30, 379.
13. Brett, J. R. & Groves, T. D. D. (1979). Physiological Energetics. New York, NY: Academic Press.
14. De Charleroy, D., Grisez, L., Thomas, K., Belpaire, C. & Ollevier, F. (1990). The life cycle of Anguillicola crassus. Diseases of Aquatic Organisms 8, 77-84.
15. Dekker, W. (2003). On the distribution of the European eel (Anguilla anguilla) and its fisheries. Canadian Journal of Fisheries and Aquatic Sciences 60, 787-799.
16. Durif, C., Dufour, S. & Elie, P. (2005). The silvering process of Anguilla anguilla: a new classification from the yellow resident to the silver migrating stage. Journal of Fish Biology 66, 1025-1043.
17. Friedland, K. D., Miller, M. J. & Knights, B. (2007). Oceanic changes in the Sargasso Sea and declines in recruitment of the European eel. ICES Journal of Marine Science 64, 519-530.
18. Fulton, T. W. (1904). The rate of growth in fishes. Fisheries Board of Scotland Annual Report 22, 141-241.
19. van Ginneken, V. J. T. & Van den Thillart, G. (2000). Physiology - eel fat stores are enough to reach the Sargasso. Nature 403, 156-157.
20. van Ginneken, V., Antonissen, E., Muller, U. K., Booms, R., Eding, E., Verreth, J. & Van den Thillart, G. (2005). Eel migration to the Sargasso: remarkably high swimming efficiency and low energy costs. Journal of Experimental Biology 208, 1329-1335.
21. Jellyman, D. & Tsukamoto, K. (2002). First use of archival transmitters to track migrating freshwater eels Anguilla dieffenbachii at sea. Marine Ecology Progress Series 233, 207-215.
22. Jessop, B. M. (2010). Geographic effects on American eel (Anguilla rostrata) life history characteristics and strategies. Canadian Journal of Fisheries and Aquatic Sciences 310, 237-244.
23. Kelly, C. E., Kennedy, C. R. & Brown, J. A. (2000). Physiological status of wild European eels (Anguilla anguilla) infected with the parasitic nematode, Anguillicola crassus. Parasitology 120, 195-202.
24. Knights, B. (2003). A review of the possible impacts of long-term oceanic and climate changes and fishing mortality on recruitment of anguillid eels of the Northern Hemisphere. Science of the Total Environment 310, 237-244.
25. Kuwahara, A., Niimi, A. & Itagaki, H. (1974). Studies of a nematode parasite in the air bladder of the eel. Descriptions of Anguillicola crassa n. sp. I (Philometridae, Anguillicolidae). Japanese Journal of Parasitology 23, 275-279.
26. Larsson, P., Hamrin, S. & Okla, L. (1990). Fat content as a factor inducing migratory behavior in the eel (Anguilla anguilla L) to the Sargasso Sea. Naturwissenschaften 77, 488-490.
27. Limburg, K. E., Wickström, H., Svedäng, H., Elfman, H. & Kristiansson, P. (2003). Do socked freshwater eels migrate? Evidence from the Baltic suggests yes. American Fisheries Society Symposium 35, 275-284.
28. McCance, R. A. (1944). The chemistry of growth and the food value of the common eel (Anguilla anguilla (L.)). Biochemical Journal 38, 474-480.
29. McCleave, J. D. & Arnold, G. P. (1999). Movements of yellow- and silver-phase European eels (Anguilla anguilla L.) tracked in the western North Sea. ICES Journal of Marine Science 56, 510-536.
30. Molnar, K. (1993). Effect of decreased oxygen content on eels (Anguilla anguilla) infected by Anguillicola crassus (Nematoda: Dracunculoidea). Acta Veterinaria Hungarica 41, 349-360.
31. Montén, E. (1985). Fish and Turbines: Fish Injuries During Passage Through Power Station Turbines. Stockholm: Vattenfall.
32. Neuman, E. & Thoresson, G. (1979). Fisket efter blankål (Anguilla anguilla L.) kring Oskarshamnsverket åren 1962-1977. Swedish Environmental Protection Agency, PM Series 1162, 45.
33. Nordquist, O. F. & Alm, G. (1920). Undersökningar om ålens ålder, storlek och tillväxthastighet i Sverige. Svenska Hydrografisk- Biologiska Kommissionens Skrifter. Fyrskeppsundersökningar 6, 1-16.
34. Palstra, A. (2006). Energetic Requirements and Environmental Constraints of Reproductive Migration and Maturation of European Silver Eel (Anguilla anguilla L.). Leiden: University of Leiden.
35. Palstra, A. P. & Van den Thillart, G. (2010). Swimming physiology of European silver eels (Anguilla anguilla L.): energetic costs and effects on sexual maturation and reproduction. Fish Physiology and Biochemistry 36, 297-322.
36. Palstra, A. P., Heppener, D. F. M., van Ginneken, V. J. T., Szekely, C. & Van den Thillart, G. (2007). Swimming performance of silver eels is severely impaired by the swim-bladder parasite Anguillicola crassus. Journal of Experimental Marine Biology and Ecology 352, 244-256.
37. Palstra, A., van Ginneken, V. & Van den Thillart, G. (2008). Cost of transport and optimal swimming speed in farmed and wild European silver eels (Anguilla anguilla). Comparative Biochemistry A 151, 37-44.
38. Pankhurst, N. W. (1982). Relation of visual changes to the onset of sexual maturation in the European eel Anguilla anguilla (L). Journal of Fish Biology 21, 127-140.
39. Peltonen, H., Raitaniemi, J., Parmanne, R., Eklund, J., Nyberg, K. & Halling, F. (2002). Age determination of Baltic herring from whole otoliths and from neutral red stained otolith cross sections. ICES Journal of Marine Science 59, 323-332.
40. Scaion, D., Belhomme, M. & Sébert, P. (2008). Pressure and temperature interactions on aerobic metabolism of migrating European silver eel. Respiratory Physiology & Neurobiology 164, 319-322.
41. Schmidt, J. (1923). Breeding places and migration of the eel. Nature 111, 51-54.
42. Schmidt-Nielsen, K. (1972). Locomotion: energy cost of swimming, flying, and running. Science 177, 222-228.
43. Sébert, P., Scaion, D. & Belhomme, M. (2009). High hydrostatic pressure improves the swimming efficiency of European migrating silver eel. Respiratory Physiology & Neurobiology 165, 112-114.
44. Sjöberg, N. B., Petersson, E., Wickström, H. & Hansson, S. (2009). Effects of the swimbladder parasite Anguillicola crassus on the migration of European silver eels Anguilla anguilla in the Baltic Sea. Journal of Fish Biology 74, 2158-2170.
45. Svedäng, H. & Wickström, H. (1997). Low fat contents in female silver eels: indications of insufficient energetic stores for migration and gonadal development. Journal of Fish Biology 50, 475-486.
46. Svedäng, H., Neuman, E. & Wickström, H. (1996). Maturation patterns in female European eel: age and size at the silver eel stage. Journal of Fish Biology 48, 342-351.
47. Svedäng, H., Wickström, H., Reizenstein, M., Holmgren, K. & Florenius, P. (1998). Accuracy and precision in eel age estimation, using otoliths of known and unknown age. Journal of Fish Biology 53, 456-464.
48. Tesch, F. W. (1978). Telemetric observations of the spawning migration of the eel (Anguilla anguilla) west of the European continental shelf. Environmental Biology of Fishes 3, 203-209.
49. Tesch, F. W. (1989). Changes in swimming depth and direction of silver eels (Anguilla anguilla L.) from the continental shelf to the deep sea. Aquatic Living Resources 2, 9-20.
50. Tesch, F. W. (2003). The Eel. Oxford: Blackwell Science.
51. Van den Thillart, G., Palstra, A. & Van Ginneken, V. (2007). Simulated migration of European silver eel; swim capacity and cost of transport. Journal of Marine Science and Technology-Taiwan 15, 1-16.
52. Videler, J. J. & Nolet, B. A. (1990). Costs of swimming measured at optimum speed: scale effects, differences between swimming styles, taxonomic groups and submerged and surface swimming. Comparative Biochemistry and Physiology 97, 91-99.
53. Vøllestad, L. A. (1992). Geographic variation in age and length at metamorphosis of maturing European eel: environmental effects and phenotypic plasticity. Journal of Animal Ecology 61, 41-48.
54. Vøllestad, L. A. & Jonsson, B. (1986). Life history characteristics of the European eel Anguilla anguilla in the Imsa river, Norway. Transactions of the American Fisheries Society 115, 864-871.
55. Ware, D. M. (1982). Power and evolutionary fitness of teleosts. Canadian Journal of Fisheries and Aquatic Sciences 39, 3-13.
56. Wenner, C. A. & Musick, J. A. (1974). Fecundity and gonadal observations of the American eel, Anguilla rostrata, migrating from Chesapeake Bay, Virginia. Journal of the Fisheries Research Board of Canada 31, 1387-1391.
57. Westerberg, H., Lagenfelt, I. & Svedäng, H. (2007). Silver eel migration behaviour in the Baltic. ICES Journal of Marine Science 64, 1457-1462.
58. Wickström, H. (1986). Studies in the European eel by the Institute of Freshwater Research 1977-85. Information From the Institute of Freshwater Research, Drottningholm 13 (in Swedish with English summary).
59. Wickström, H., Höglund, J. & Clevestam, P. D. (1998). The spreading of Anguillicola crassus in fresh water lakes in Sweden. Bulletin Francais de la Pêches et la Pisciculture 349, 215-221.
60. Wootton, R. J. (1979). Energy cost of egg production and environmental determinants of fecundity in teleost fishes. Symposium of the Zoological Society of London 44, 133-159.
61. Wootton, R. J. (1990). Ecology of Teleost Fishes. London: Chapman & Hall.
62. Anon. (1998). Commission Directive 98/64/EC of 3 September 1998 establishing Community methods of analysis for the determination of amino acids, crude oils and fats, and olaquindox in feeding stuffs amending Directive 71/393/EEC. In Official Journal of the European Communities. Available at
63. Burgerhout, E., Brittijn, S. A., Palstra, A. P. & Van den Thillart, G. E. E. J. M. (2010). Swimming trials with male silver eels indicating a higher efficiency by swimming in groups. In Proceeding of the Fitfish - Workshop on the Swimming Physiology of Fish. Barcelona, 2-3 July 2010. Available online October 2010 at
64. Clevestam, P. D. & Wickström, H. (2008). Rädda ålen och ålfisket! - Ett nationellt bidrag till en europeisk förvaltningsplan. Vetenskaplig slutrapport från pilotprojekt till Fonden för fiskets utveckling. Swedish Board of Fisheries. Dnr: 231-1156-1104 (in Swedish). Available at
65. ICES (2006). Report of the 2006 session of the joint EIFAC/ICES working group on eels. FAO European Inland Fisheries Advisory Commission; International Council of the Exploration of the Sea, Rome 23-27 January 2006. EIFAC Occasional Paper. No. 38, ICES CM 2006/ACFM:16, p. 352. Available at
66. ICES (2010). Report of the 2010 session of the Joint EIFAC/ICES Working Group on Eels. FAO European Inland Fisheries Advisory Commission; International Council for the Exploration of the Sea. Hamburg, Germany, 9-14 September 2010. EIFAC Occasional Paper. No. 41. ICES CM 2010/ACOM:18, 721. Available at