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The European Eel (Anguilla Anguilla, Linnaeus), Its Lifecycle, Evolution and Reproduction: a Literature Review

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The European Eel (Anguilla Anguilla, Linnaeus), Its Lifecycle, Evolution and Reproduction: a Literature Review Rev Fish Biol Fisheries (2005) 15:367–398 DOI 10.1007/s11160-006-0005-8 RESEARCH ARTICLE The European eel (Anguilla anguilla, Linnaeus), its lifecycle, evolution and reproduction: a literature review Vincent J. T. van Ginneken Æ Gregory E. Maes Received: 1 March 2005 / Accepted: 3 January 2006 Ó Springer Science + Business Media B.V. 2006 Abstract The European eel (Anguilla anguilla (allozymes, mitochondrial DNA and anonymous Linnaeus 1758) is a species typical for waters of genomic-DNA. Although recognised as two dis- Western Europe. Thanks to early expeditions on tinct species, it remains unclear which mecha- the Atlantic Ocean by the Danish biologist nisms play a role in species separation during Johannes Schmidt who found small (<10 mm) larval drift, and what orientation mechanism eels leptocephali larvae in the Sargasso Sea about use during migration in the open sea. The current 100 years ago, we have now a strong indication status of knowledge on these issues will be pre- where the spawning site for this species is lo- sented. The hypothesis that all European eel cated. The American eel (Anguilla rostrata, migrate to the Sargasso Sea for reproduction and LeSueur) also spawns in the Sargasso Sea. The comprise a single randomly mating population, spawning time and location of both species have the so called panmixia theory, was until recently been supported and refined in recent analyses of broadly accepted. However, based on field the available historical data. Subsequent ichthy- observations, morphological parameters and oplankton surveys conducted by McCleave molecular studies there are some indications that (USA) and Tesch (Germany) in the 1980s indi- Schmidt’s claim of complete homogeneity of the cated an increase in the number of leptocephali European eel population and a unique spawning <10 mm , confirming and refining the Sargasso location may be an overstatement. Recent Sea theory of Johannes Schmidt. Distinctions molecular work on European eel indicated a between the European and American eel are genetic mosaic consisting of several isolated based on morphological characteristics (number groups, leading to a rejection of the panmixia of vertebrae) as well as molecular markers theory. Nevertheless, the latest extensive genetic survey indicated that the geographical compo- nent of genetic structure lacked temporal stabil- V. J. T. van Ginneken (&) ity, emphasising the need for temporal Integrative Zoology, van der Klaauw Laboratorium, replication in the study of highly vagile marine Institute Biology Leiden, PO Box 9511, 2300RA Leiden, The Netherlands species. Induced spawning of hormone treated e-mail: [email protected] eels in the aquarium was collective and simulta- neous. In this work for the first time group G. E. Maes spawning behaviour has ever been observed and Laboratory of Aquatic Ecology, Katholieke Universiteit Leuven, Ch. de Deberiotstraat 32, B-3000 recorded in eels. Studies in swim-tunnels indicate Leuven, Belgium that eels can swim four to six times more 123 368 Rev Fish Biol Fisheries (2005) 15:367–398 efficiently than non-anguilliform fish such as heat develops, it induces putrefaction.’’ (Bertin trout. After a laboratory swim trial of eels over 1956). Until the early 20th century, one could 5,500 km, the body composition did not change reasonably speak of the mysterious life of the eel. and fat, protein and carbohydrate were used in Thanks to the early marine expeditions of the the same proportion. This study demonstrated Danish biologist Johannes Schmidt (see Fig. 2 for for the first time that European eel are physio- sampling stations for larvae) the central mystery logically able of reaching the Sargasso Sea with- of its breeding location has been elucidated out feeding. Based on catches of newly hatched (Schmidt 1922, 1923, 1925, 1935). Schmidt based larvae, temperature preference tests and telem- his conclusion regarding the spawning site of etry tracking of mature hormone treated ani- the European eel in the Sargasso Sea (Fig. 1) on mals, it can be hypothesised that spawning in the larvae (Lepocephali) distributions (see Section Sargasso Sea is collective and simultaneous, ‘‘The location of the spawning areas’’). while presumably taking place in the upper Despite the intensive research on eels follow- 200 m of the ocean. Successful satellite tracking ing the work of Schmidt (1923, 1925, 1935), there of longfin female eels in New Zealand has been are many uncertainties, and there is still a lack of performed to monitor migration pathways. knowledge on many aspects of the life cycle of the Implementation of this new technology is possi- European eel. This is best summarised in the ble in this species because it is three times larger book of Harden Jones (1968): ‘‘No adult eels have than the European eel. In the future, miniaturi- ever been caught in the open Atlantic nor eggs sation of tagging technology may allow European definitely identified in the wild. Migration routes eels to be tracked in time by satellite. The most and spawning conditions for adults are unknown interesting potential contribution of telemetry or conjectural, as are many details of the devel- tracking of silver eels is additional knowledge opment, feeding and growth of larvae. Mecha- about migration routes, rates, and depths. In nisms for species separation (note: separation combination with catches of larvae in the Sar- between the American eel and the European eel) gasso Sea, it may elucidate the precise spawning during larvae migration are speculative, and de- locations of different eel species or groups. Only tails of larval migration or drift are uncertain’’. then, we will be able to define sustainable man- In this review we will present the progress in agement issues by integrating this novel know- knowledge and new insights about the eel life ledge into spawners escapement and juvenile cycle following the initial work of Schmidt at the fishing quota. beginning of the previous century. This new information is based on the application of new Keywords Anguilla Æ Migration Æ Sargasso Sea Æ techniques and methodologies such as refined and Molecular studies Æ Spawning behaviour Æ improved catching techniques for ichthyoplank- Satellite ton surveys, new molecular DNA analyses, telemetry-tracking studies, endocrinological sur- Introduction veys in field studies, energy balance studies in large swim-tunnels, and behavioural studies of Although a large amount of scientific literature hormone treated animals. has been produced on freshwater eels (Anguilla sp.; see e.g. references of this review), major questions still have to be resolved mainly on the Eel life cycle and fisheries topic of spawning grounds and reproduction. Al- ready around 350 BC Aristotle wrote in his The life-history of the European eel (Anguilla ‘Historia Animalium’: ‘‘the eels come from what anguilla L.) depends strongly on oceanic condi- we call the entrails of the earth. These are found in tions; maturation, migration, spawning, larval places where there is much rotting matter, such as transport and recruitment dynamics are completed in the sea, where seaweeds accumulate, and in the in the open ocean (Tesch 2003). Partially mature rivers, at the water’s edge, for there, as the sun’s adults leave the continental rivers at different 123 Rev Fish Biol Fisheries (2005) 15:367–398 369 Fig. 1 Distribution patterns of eel larvae with the size of the larvae in mm (source: Schmidt 1923) times, strongly dependent on lunar phase and corresponds to approximately 2 to 2.2 billion atmospheric conditions (Desaunay and Gue´rault Euros per year (Heinsbroek 1991). 1997; Okamura, Yamada, Tanaka, Horie, Utoh, Eel populations have been declining worldwide Mikawa, Akazawa, Oka 2002; Tesch 2003), swim over the last decade (Stone 2003). European eel southward using the Canary and North-equatorial (Anguilla anguilla) numbers have dropped as currents and arrive 6–7 months later at the Sar- much as 99% since the early eighties of the pre- gasso Sea to spawn and then die. The leptocephali vious century, while Japanese eel (Anguilla larvae are transported along the Gulf Stream and japonica) dropped as much as 99% since the early North-Atlantic Drift for a journey of 8–9 months seventies of the previous century (Dekker, back to the eastern Atlantic coast (Lecomte-Fini- 2003b). North-American eels are suffering steep ger 1994; Arai et al. 2000), where they metamor- drop-offs as well (Fig. 3a). phose to glass eels, ascent rivers and grow till Also the trends in glass eel recruitment to the partial maturity, 6–10 years later (Tesch 2003). European continent show steep declines from the A total of 25,000 tons of eels are consumed in eighties of the previous century (Fig. 3b). Europe annually (Usui 1991). Eel fisheries in The exact cause for this phenomenon is Europe cover an area of 90,000 km2 with unknown, but possible causes include: (a) con- approximately 25,000 people generating income tamination with toxic PCBs, which are released from eel fisheries and aquaculture (Dekker 1998, from fat stores during their long-distance migration 2003a, 2004). On a worldwide scale eel (fisheries and interfere with reproduction (Castonguay et al. and fish culture) was estimated to produce be- 1994); (b) infection with the swimbladder parasite tween 100,000 to 110,000 tons in 1987, which Anguillicola crassus (Haenen 1995); (c) viruses 123 370 Rev Fish Biol Fisheries (2005) 15:367–398 Fig. 2 Principal Danish collection stations of eel larvae, 1903–1922 (After: Schmidt 1925). Closed circles indicate stations by research ships and open circles those by other ships (source: Vladykov 1964) (van Ginneken et al. 2004, 2005a), (d) catches of larvae eels in relation to size and age. oceanographic/climatic changes (Knights 2003); Johannes Schmidt gathered records of over 10,000 (e) diminished fat stores due to insufficient food European eel larvae and about 2,400 American eel supplies in the inland waters (Sveda¨ng and Wick- larvae over a period of 25 years.
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