Journal of Fish Biology (2012) 81, 365–386

doi:10.1111/j.1095-8649.2012.03373.x, available online at wileyonlinelibrary.com

The Anguilla spp. migration problem: 40 million yearsof evolution and two millennia of speculation

D. Righton*†, K. Aarestrup‡, D. Jellyman§, P. Sebert‖, G. van denThillart¶ and K. Tsukamoto**

*Centre for Environment, Fisheries and Aquaculture Science, Pakefield Road, Lowestoft NR330HT, U.K., ‡Technical University of Denmark, National Institute of Aquatic Resources,

Vejlsoevej 39, DK-8600 Silkeborg, Denmark, §Freshwater Fisheries, NIWA, P. O. Box 8602,Christchurch 8440, New Zealand, ‖EA4324-ORPHY, UFR Sciences, 6, Avenue Le Gorgeu, CS

93837, 29238 Brest Cedex 3, France, ¶Leiden University, Institute of Biology, GorlaeusLaboratories, Postbus 9502, 2300 RA Leiden, the Netherlands and **Atmosphere and Ocean

Research Institute, The University of Tokyo 5-1-5, Kashiwanoha, Kashiwa, Chiba277-8564, Japan

Anguillid eels Anguilla spp. evolved between 20 and 40 million years ago and possess a numberof remarkable migratory traits that have fascinated scientists for millennia. Despite centuries ofeffort, the spawning areas and migrations are known only for a few species. Even for these species,information on migratory behaviour is remarkably sketchy. The latest knowledge on the requirementsfor successful migration and field data on the migrations of adults and larvae are presented, howexperiments on swimming efficiency have progressed the understanding of migration are highlightedand the challenges of swimming at depth considered. The decline of Anguilla spp. across the world isan ongoing concern for fisheries and environmental managers. New developments in the knowledgeof eel migration will, in addition to solving a centuries old mystery, probably help to identify howthis decline might be halted or even reversed. © 2012 Crown Copyright

Journal of Fish Biology © 2012 The Fisheries Society of the British Isles

Key words: anguillid; behaviour; eel; leptocephalus; silver eel; swimming.

INTRODUCTION

Anguillid eels Anguilla spp. are mysterious creatures. They are born in remote partsof the world’s tropical oceans, drift over a period of months to years to the continentalshelf, then migrate into fresh water where they spend up to a century or more, finallyslipping back into the ocean depths to find again their birthplace and contribute tothe next generation (Tesch, 1977, 2003). Scientists have long quested to discoverthe secrets of eel migration. The case of the European eel Anguilla anguilla (L.1758) is well documented, beginning with the musings of Aristotle (350 B.C.), whoclaimed in his History of Animals that eels originated from ‘the bowels of the earth’.It took another 2000 years before the discoveries of Grassi (1896), who identifiedthe larval form of eels, and Schmidt (1912), who used this knowledge to find the

†Author to whom correspondence should be addressed. Tel.: +44 (0) 1502 524359; email: david.righton@cefas.co.uk

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densest aggregations of larvae, helped to identify where A. anguilla spawned andclosed the migratory loop. Discovery of the spawning area of other Anguilla spp.has been similarly protracted (e.g. in the case of Japanese eel Anguilla japonicaTemminck & Schlegel 1846 and marbled eel Anguilla marmorata Quoy & Gaimard1824, Tsukamoto et al., 2011), and for some species the larvae have never beendiscovered (New Zealand longfin eel Anguilla dieffenbachii Gray 1842, Jellyman &Bowen, 2009). In consequence, a rich folk history surrounds Anguilla spp. (Fort,2003; Prosek, 2010).

Even today, with the advent of marine remote sensing, genetic and otolith analyses,electronic tagging, and investigative computer modelling, there are many fundamen-tal questions about Anguilla spp. migrations that remain unanswered. The recentdeclines in Anguilla spp. populations (Dekker, 2003) make gaining more insightinto their migration increasingly urgent because it will help to identify the extentto which changes in the management of Anguilla spp. stocks and habitat can helpto conserve and recover stock biomass. In the following review, a number of thesequestions are identified, the evidence collected to date presented, and the directionsfor future research outlined. Most of attention is focused on those Anguilla spp. forwhich oceanic studies have been undertaken. Of necessity, this excludes the Amer-ican eel Anguilla rostrata (LeSueur, 1817), for which the down-river and oceanicmigrations are poorly understood. A new study of seaward migration in silver A.rostrata is given by Verreault et al. (2012).

FROM PREPUBESCENT TO SEXUALLY MATURE SILVER EELIN A FEW MONTHS: WHAT IS THE METAMORPHOSIS PROCESS?

Anguilla spp. live a relatively sedate life in the growth phase, which, in the caseof A. dieffenbachii (Todd, 1980), can last between 2 and >100 years. In the monthsbefore the onset of the oceanic migration, however, they need to start adapting to theenvironment they will be subjected to and they must adapt accordingly (Rousseauet al., 2009). This involves a complex process of hormonal, morphological, physi-ological and behavioural changes that provide the capability for the fishes to facethe extreme swimming ahead. This process is called silvering. Despite its name,silvering is not just a superficial change in colour, but a suite of physiological andmorphological changes that pre-adapts Anguilla spp. to the next stage of their life.

All freshwater Anguilla spp. are presumed to spawn at sea, and adaptation to lifein the ocean is hormonally driven, mediated by the gonadotropic and corticotropicaxes (Aroua et al., 2005). Morphological changes during silvering include the devel-opment of a thicker skin, production of mucus to protect it and a change in colourfrom brown or green. The dorsal and lateral surfaces become darker while the depo-sition of purines in the scales of the ventral surface make the belly takes on a silveryappearance. While the dorsal colours can vary, the important feature that is retainedis the counter-shading colouration that is typical of oceanic pelagic fishes, whichreduces the risk of detection by predators: the dark dorsal surface makes it difficultfor predators at shallower depths to spot Anguilla spp. against the dark backgroundbelow, and vice versa for predators at greater depths. Beyond colouration, there areseveral other major physical adaptations. Perhaps, the most obvious external change

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is the enlargement of the eyes by up to 50% that, along with an increase in the num-ber of rods on the retina and an increase in rhodopsin pigment relative to porphyrin(Rousseau et al. 2009), allows Anguilla spp. to see at very low light levels. Theseexternal morphological changes occur at the same time as changes that take placeinternally that enable efficient and sustained swimming.

Firstly, to enable Anguilla spp. to swim the great distances they need to achieve,they need to have sufficient fuel to power them since, once silvered, Anguilla spp.no longer ingest food because the gut ceases to function in digestion i.e. fishes maketheir spawning migration under conditions of starvation (Tesch, 2003; Chow et al.,2010). To this end, fat content increases dramatically and is deposited in muscles,under the skin and in the liver. Fat content reaches its maximum between 25 and 30%of body mass, comparable (if not greater than) the maximum observed in farmedAtlantic salmon Salmo salar L. 1758 (van Ginneken & Maes, 2005). This energystore is fundamental for the long migration ahead because without sufficient fat,Anguilla spp. may be unable to complete the migration at all or they may not beable to produce enough good quality gametes at the end of their journey to thespawning grounds (Tsukamoto, 2009).

Secondly, to enable efficient swimming, the specialized organ that controls buoy-ancy, the swimbladder, also becomes more vascularized and its walls become thicker.These adaptations enable better gas secretion and retention, so that any requiredchanges in buoyancy while in the ocean can be achieved quickly and efficiently. Thegas secretion capability of the swimbladder is increased by an increase in vascular-ization in the rete mirabile. At the same time, guanine is deposited in the walls of theswimbladder, which acts to reduce gas loss by diffusion (Kleckner, 1980; Kleckner& Krueger, 1981).

Thirdly, Anguilla spp. must adjust their ionoregulatory and osmoregulatory pro-cesses for a life in seawater rather than fresh water. Teleosts regulate the osmoticconcentration of their body fluids at c. 30–40% of the level of oceanic seawater.Fishes in fresh water, therefore, must deal with the osmotic entry of water and diffu-sional loss of salts via the gills and gut. To compensate, they produce large volumesof dilute urine. Marine fishes have the opposite problem of osmotic loss of waterand diffusional entry of salts. As a consequence, marine fishes drink seawater andexcrete excess salts. While most fish species are adapted to live in only one environ-ment or the other (stenohaline), Anguilla spp. [like European flounder Platichthysflesus (L. 1758)] are able to move into seawater at any time, despite their longevityin freshwater habitats. This ability of Anguilla spp. to move between seawater andfresh water relies of the capabilities of the organs that regulate water balance (thegills, gut and kidney) and the tissues (principally the adrenal gland) that produce thehormones to control the diffusion of water into or out of the body (Rankin, 2009).

At no point during the silvering process do Anguilla spp. become sexually mature.This final phase of the fish’s transformation does not take place until the oceanicjourney is underway. The development of maturation protocols for cultured Anguillaspp. has provided information about some of the physical and physiological changesassociated with maturation (Boetius & Boetius, 1967; van den Thillart & Dufour,2009) but, because the final part of Anguilla spp’s lives is so difficult to study undernatural conditions, the natural process of sexual maturation remains almost unknown.A few pre-spawning Anguilla spp. have been caught at sea and show more advancedmaturation than in fresh water while the handful of post-spawned fishes caught have

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all been completely spent with advanced muscle wastage (Tsukamoto et al., 2011),indicating they do not survive spawning.

THE PHYSIOLOGY OF ANGUILLA SPP. SWIMMING: HOW DO THEYACHIEVE SUCH LONG MIGRATIONS?

More than 50 years ago, Tucker (1959) raised doubts whether A. anguilla wouldbe able to swim across the Atlantic Ocean based on simple energetic arguments.The long distance, he stated, would cost too much energy, and A. anguilla eels weresimply A. rostrata eels gone adrift. In 1972, Schmidt-Nielsen (1972) calculated thecost of transport for salmonids to 2 kJ kg−1 km−1 and, based on that figure, it wassuggested that Anguilla spp. would need at least 300 g fat per kg body mass to crossthe Atlantic Ocean. Although some Anguilla spp. might reach a body fat content of30%, most have only c. 20% body fat (Svedang & Wickstrom, 1997), so there issome merit in the first part of Tucker’s (1959) argument. Much of Tucker’s argument,however, has long since proved inaccurate: A. anguilla have been proved distinctfrom A. rostrata through the use of protein electrophoresis and genetic studies (Com-parini & Rodino, 1980; Williams & Koehn, 1984; Avise et al., 1986, 1990; Tagliaviniet al., 1995; Nieddu et al., 1998). Thus, with Tucker’s (1959) objections largely dealtwith, the swimming capability and efficiency of Anguilla spp., which has developedover the last 10–20 million years (Inoue et al., 2010), began to be investigated.

Although some early work on swimming efficiency was undertaken (Webb, 1971;McCleave, 1980), much of the research in this field has been undertaken by van Gin-neken and van den Thillart (2000), van den Thillart et al. (2004), van Ginneken andMaes (2005) and Palstra et al. (2008) using 2 m long Blazka type swimming tun-nels. This piece of equipment generates a continuous flow of water through a centralswimming chamber. Once a fish is placed inside the chamber, its rate of swimmingcan be adjusted and the rate of depletion of oxygen in the chamber (over a certainperiod of time) is used to calculate energy consumption. In contrast to theoreticalstudies of swimming that suggested anguilliform swimming is inefficient comparedto, for example, salmonids (Videler, 1993; Bone et al., 1995), the first ever trials withA. anguilla showed quite the opposite. In a long-distance swimming trial, five silverA. anguilla of c. 0·75 m in total length (LT) were swum for 95 days at 0·5 LT s−1,corresponding to a swimming distance of 2850 km (van den Thillart et al., 2004).This demonstrated that A. anguilla had an impressive endurance capacity and sug-gested that they would be able to cover the distance between Europe and the SargassoSea within the 6 months between the onset of migration and peak spawning.

The second aspect of swimming ability, efficiency, has also been established inrecent years. A range of different experiments were undertaken to determine thecost of transport (COT) of A. anguilla at various swimming speeds. Based on aten-day swim trial, van Ginneken & van den Thillart (2000) demonstrated that theCOT of silver A. anguilla swimming at 0·4 LT s−1 is extremely low: 0·575 J g−1

km−1, much lower than the equivalent O2 consumption of S. salar (van Ginneken& Maes, 2005), and some 0·3–0·4 the values reported in the literature for otherspecies (Schmidt-Nielsen, 1972). This showed beyond doubt that A. anguilla arevery efficient endurance swimmers. Other experiments have shown that the optimalspeed of A. anguilla might even enable them to swim to the Sargasso Sea from the

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westernmost coasts of Europe within 3·5 months instead of 6 months (Palstra et al.,2008). Evidently, even when they might take up to 5 months from some of the moredistant parts of Europe, there would still be enough time to complete the maturationprocess and find mates. Crucially, the results from the swim-tunnel experiments haveshown empirically that A. anguilla can migrate at speeds and with an efficiency thatdoes not completely exhaust fat reserves and will enable them to complete theirsexual maturation in time to produce viable gametes and spawn at the end of theirlong journey.

SEXUAL DIMORPHISM AND MIGRATION

Male Anguilla spp. are, when they migrate, generally smaller than females. Whilethis reflects the requirement for relative investment in gametes, the smaller sizeof males presents some interesting questions. Their relative rate of swimming (inLT s−1) will have to be greater than that of females to reach the spawning area atthe same time; alternatively, if they swim slower, they will need to leave fresh waterearlier than females to coincide with their arrival at the spawning area. What effectmight this have on the costs of transport or efficiency of swimming? Recent physio-logical work has shown that the energetic capability of male and female A. anguillamuscle tissue differs, with male tissue being most efficient at greater depths (Scaionet al., 2008). Several authors have suggested, therefore, that understanding the ener-getic of males and females is of critical importance (Belpaire et al., 2009; Kettleet al., 2011). Although most swim-tunnel experiments have been undertaken onfemales, the swimming efficiency of males has begun to be investigated in recentyears. Quintella et al. (2010) compared the critical swimming speed and found that,when expressed in LT s−1, the critical swimming speed (above which fishes cannotmaintain continuous swimming behaviour) of males is c. 50% higher than in females(1·7 v. 1·2) allowing them to achieve the same ground speed as females (0·7 m s−1).To support this result, recent experiments have shown that male silver A. anguillacan swim at the same COT and at similar speeds as females, i.e. up to 0·6 m s−1

(E. Burgerhout, C. Tudorache & G. van den Thillart, unpubl. data).Field data on the swimming behaviour of males is lacking: all satellite tracking

experiments have been undertaken using female silver Anguilla spp. This is simplybecause females, by virtue of their greater size, are less likely to be affected by theattachment of the tag. The ratio between the size of the tag and the tagged fish isa primary consideration in all tagging studies (McCleave & Stred, 1975; Baras &Jeandrain, 1998), and most male Anguilla spp. are simply too small to attach the cur-rent generation of satellite tags. There is, therefore, almost no information availableon the natural swimming behaviour of male Anguilla spp., other than observations ofthe timing of migration. Migratory male A. dieffenbachii appear to depart from freshwater a month earlier than females (Todd, 1981), presumably because they will swimslower than females and therefore need to start their migration earlier, or perhapsbecause males take longer to reach full sexual maturity, and therefore need a longeroceanic migration period. This may also hold true for A. anguilla: based on swim-ming tunnel trials, estimates of the duration of migration of male A. anguilla were174 days v. 139 days for females (van Ginneken & Maes, 2005), and there is someevidence that the timing of departure of males and females also differs (Tesch, 2003).

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THE OCEANIC SPAWNING MIGRATION: WHAT DO ANGUILLA SPP.DO ALL DAY?

While the laboratory studies of Anguilla spp. swimming showed that they arephysically capable of reaching their far-flung spawning areas, they do not provideevidence that they can achieve this feat under natural oceanic conditions, wherecounter-currents, navigational issues, predators and more await. Direct studies of theswimming behaviour of Anguilla spp. became possible with the advent of acoustictracking in the 1960s. This technology involves the use of an acoustic transmit-ter that is attached to, or implanted in a fish. The regular transmissions from thetag are detected using a directional hydrophone or scanning sonar devices (Tesch,1989, 1995; McCleave & Arnold, 1999). Following tagged Anguilla spp. that maybe hundreds of metres below the sea surface with monitoring equipment onboarda vessel capable of working at sea is both difficult and expensive, and often onlyresults in a few hours or days of data being collected for each individual. More-over, only one individual can be followed at a time. Despite these disadvantages,early studies provided significant information on swimming directions and speeds.For example, silver A. anguilla tracked in inshore marine areas showed evidence ofdaily vertical migrations, ascending at dusk and descending at dawn (Tesch, 1978,1989, 1995; Westerberg, 1979; Tesch et al., 1991), with maximum depths recordedbeing 700 m (Tesch, 1989). Observed swimming speeds varied considerably, rang-ing from 12 km day−1 (Tesch, 1978) to 48 km day−1 (Tesch, 1974; McCleave &Arnold, 1999). Experiments have also been conducted with partially matured (hor-mone treated) fish that were released in the vicinity of possible spawning areas.Anguilla anguilla released in the Sargasso Sea did not descend beyond 300 m (Fricke& Kaese, 1995), while A. japonica released near sea mounts swam at depths rangingfrom 81 to 172 m (Aoyama et al., 1999). None of these tracking trials producedsignificant advances in the knowledge of likely spawning areas, partly because itwas not feasible to track a large number of individuals and because tracking becameincreasingly difficult as fishes travelled further from the release site.

Much less is known about the behaviour of Anguilla spp. once they leave coastalwaters and move into deeper, oceanic waters, for several reasons. Firstly, the migra-tion routes of virtually all Anguilla spp. are unknown, and as a consequence virtuallyall attempts to capture fishes in the ocean have failed, with the notable recentexceptions in the north-west Pacific (Tsukamoto et al., 2011). Secondly, the costof oceanic fieldwork is very high, and this mitigates against large and frequentefforts to search for Anguilla spp. over large ocean expanses. Finally, the equipmentto follow Anguilla spp. over huge distances has, until recently, not been available.The advent of pop-up (satellite tracking) tags at the start of the 21st century, how-ever, offered the possibility of being able to track migrating Anguilla spp. at sea,as well as providing information on their swimming depths and speed. A majoradvantage of this technology is that, once the tagged fishes have been released,information on their swimming behaviour and migration is relayed to a satellitewhen the attached tag pops up to the sea surface; there is no requirement for avessel to follow the fish, or a fisherman to catch and return a tag. The first use ofthese tags was with female A. dieffenbachii (Jellyman & Tsukamoto, 2002) cho-sen partly because nothing was known of likely spawning areas of this species,but also because the fish were large (1·3 m to 1·5 m LT) and would therefore be

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less affected by the presence of an external tag than would smaller species such asA. japonica.

The primary motivation for attaching satellite tags to A. dieffenbachii was todetermine migration route and spawning location. The maximum tag retention timeachieved in the studies of A. dieffenbachii to date was estimated at 161 days, bywhich time the fish had reached c. 160 km north-east of New Caledonia (>2000 km),providing the first definitive evidence that this species moves to the tropics to spawn.Other tags were not retained for as long, but their pop-off locations were consistentwith this northwards migration at a rate of between 20 and 25 km day−1 (Jellyman &Tsukamoto, 2005). Further tagging experiments have supported these initial findings(Jellyman & Tsukamoto, 2010).

The success of the A. dieffenbachii tagging experiments has encouraged othersto follow: female silver A. anguilla were first tracked in 2006 (Aarestrup et al.,2009), and silver A. japonica were tracked for the first time in 2008 (Manabe et al.,2011). Aarestrup et al. (2009) reported that speed over the ground of A. anguillawas between 5 and 25 km day−1, which was consistent with earlier experimentswhere boat-tracking studies gave speeds between 20–40 km day−1 (Tesch, 1989)and 19–50 km h−1 (McCleave & Arnold, 1999). Unlike the earlier experiments,the swimming speeds reported in Aarestrup et al., (2009) were calculated fromA. anguilla that migrated up to 1300 km from their release point, and so were,like Jellyman & Tsukamoto (2005), a measure of the endurance swimming capabil-ity of Anguilla spp. Care must be taken not to confuse travel speed with swimmingspeed; the speeds derived from a release and a pop-off position does not take intoaccount whether the fish is swimming with the benefit or hindrance of currents,or whether more convoluted route is taken than a straight line. In the case of A.anguilla, the mapped trajectory was aimed south and west into the prevailing north-wards flowing shelf-edge current, and towards the westflowing currents to the westof Africa and which continue to the west as part of the subtropical gyre system(Aarestrup et al., 2009). In contrast, tagged A. japonica did not travel such a directroute towards the spawning area (Manabe et al., 2011), but instead travelled withinthe east and north-flowing Kuroshio Current. This route, while seemingly at oddswith efficient swimming towards the spawning area to the east of the release posi-tion, may have enabled the fish to take advantage of the Kuroshio ‘conveyor belt’,which flows up to 1 m s−1 (86 km day−1) at between 200 to 400 m depth. Manabeet al. (2011) reported speeds of travel of between 28 and 80 km day−1, speeds thatare well in excess of the critical swimming speed of the larger A. anguilla. Aftertaking the advantage conferred by the Kuroshio Current into account, however, theseestimates of swimming speed were lowered to 3·4 from 12·8 km day−1, indicatingthat the current may have enhanced swimming speed by between three and eighttimes. Despite these encouraging results, it is important to note that, while satellitetags have advanced the understanding of Anguilla spp. migration considerably, caremust be taken when interpreting swimming speeds because the drag of an exter-nally attached tag may increase the cost of swimming, and thereby decrease averageswimming speeds (Burgerhout et al., 2011; Methling et al., 2011)

Although satellite tagging has not yet revealed the location of spawning locationsfor any Anguilla spp., they also provide other information on swimming behaviourbecause the tags record and transmit the depths and temperatures that the fishes expe-rience. Early temperature sensing tags deployed on A. dieffenbachii provided clear

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evidence from daily temperature shifts of some diel vertical movement in the watercolumn. Subsequent trials (Jellyman & Tsukamoto, 2005, 2010) were more success-ful, and generated considerable information on swimming depths, speeds and ascentlocations. Migrating A. dieffenbachii showed a consistent diving pattern, descendingduring the day to depths up to 900 m, while ascending at night to depths as shallowas 50 m. As distance from the coast increased, the fish swam to greater depths, espe-cially during the day, when they consistently encountered temperatures of 6–7◦ C.At night, the depth that fish occupied were relatively consistent, with the consequencethat the temperatures the fish experienced gradually increased as they made progresstowards the tropics. Similarly to A. dieffenbachii, large vertical migrations were a sig-nificant feature of the oceanic migrations of A. anguilla (Aarestrup et al., 2009) andA. japonica (Manabe et al., 2011). Anguilla anguilla moved daily across depth rangesof 200 m (night) to 1000 m (day) and temperature ranges of 6◦ C (A. anguilla: 7–13◦

C, although recent experiments have shown that, over the entire migration, this rangeis much greater, at 1–18◦ C; D. Righton, unpubl. data). These ranges were 100 and800 m and 18◦ C (4–22◦ C) for A. japonica. Again, as fishes of both species migratedfurther offshore, the depths occupied during the day increased, while night-timeoccupied depths were typically <300 m and relatively consistent over time (Fig. 1).

Initially, it was suggested that the diel diving pattern was primarily a response topredator avoidance (Jellyman & Tsukamoto, 2002), as a number of predatory fishesand whales are known to dive to the depths where the A. dieffenbachii swam dur-ing daytime. A second possible explanation for the daily dives is that fish travel asdeep as possible to avoid predators but their continued residence in low tempera-tures reduces their swimming efficiency. To offset this inefficiency, Anguilla spp.may require a daily ascent to warmer water to increase metabolic rate and muscleefficiency (Jellyman & Tsukamoto, 2005). This explanation is also offered by Scaionet al. (2008), Aarestrup et al. (2009) and Manabe et al. (2011) for A. anguilla andA. japonica, respectively. Aarestrup et al. (2009) went further, suggesting that, whileswimming in shallow warm water was beneficial for swimming activity, diving intocooler waters was necessary to delay gonad development until later in the migra-tion. Jellyman & Tsukamoto (2010) expanded on this, noting that, for females atleast, ovary development is accompanied by a dramatic increase in girth, somethingthat would significantly reduce swimming efficiency. Overall, it seems unlikely thatthere is a single driver for these diel migrations: the spawning migration strategy ismore likely to involve tradeoffs between this temperature preference for warm water[17–20◦ C (Haro, 1991)], the need to avoid predators, the need to control the onsetof maturity and the need for energy conservation. All these evolutionarily obtainedadvantages are the result of behavioural characteristics that have been driven by asimple negative phototaxis of adults.

DARING TO GO DEEP: HOW ANGUILLA SPP. RESPOND TO HIGHPRESSURES

Pressure and temperature are environmental and thermodynamic factors that modifyfish physiology. Increased pressure can inhibit or stimulate reaction rates dependingon the chemical reaction in question (Sebert et al., 2004). In contrast, an increase intemperature will always increase the rate of a reaction (as described by the Arrhenius

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0(a)

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Fig. 1. Habitat use of Anguilla anguilla in the Atlantic Ocean. (a) An example showing how the verticalmovements of A. anguilla in the ocean appear to be synchronized to dawn and dusk; (b) an example ofthe frequency distribution of depth from a week in the migration of A. anguilla occupied deep water. Thedata were collected using satellite tags attached to the dorsal surface of two individuals (as for Aarestrupet al., 2009).

reaction). Considering that during their migration Anguilla spp. will encounter tem-peratures ranging from 4 to 20◦ C and depths from 1 to (possibly) 200 atmospheres,they must have evolved physiological mechanisms to cope with the stresses that theirbehaviour and environment apply to them. Pressure and temperature can affect all theevents leading to red muscle contraction which largely drives sustained swimmingactivity. As a fish is exposed to hydrostatic pressure, swimming movements becomeless co-ordinated as the muscles become less able to function normally. As pressurecontinues to increase, smooth swimming behaviour becomes impossible, and themuscles begin to twitch before finally, as the pressure threshold (Ptr, expressed as adepth of muscle twitch in m) is reached, the muscles convulse uncontrollably. ThePtr corresponds, essentially, to a loss of muscle control. In experiments in which A.anguilla were exposed to a compression rate of c. 20 m min−1, the Ptr for yellowA. anguilla was c. 420 m at 15◦ C but 910 m at 9◦ C; for silver A. anguilla, the Ptr

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was c. 750 m at 15◦ C but 1420 m at 9◦ C (Sebert, 2008). These studies, and extrap-olations from the data, suggests that the maximum depth for A. anguilla migration isprobably in the range of 2000–2200 m (Sebert, 2008), a value far in excess of thatof most fish species but in line with the results of satellite-tagging studies. Despitethe numerous effects of pressure, Anguilla spp. muscle works well under pressure.Indeed, results from deep-sea arrow tooth eel Histiobranchus bathybius (Gunther1877) show that swimming speed under pressure require much less power. Similarreasoning for A. anguilla suggests that the mass of swimming muscle at the onset ofmigration would produce surplus power, and therefore, it might allow muscle tissueto atrophy in favour of gonad development (Sebert & Macdonald, 1993).

Experiments to assess the swimming capability of Anguilla spp. under differ-ent pressure and temperature conditions are a challenge to undertake (Nilsson et al.,1981). One option is to use a modified barochamber in combination with a swim tun-nel (Sebert et al., 2009a). A recent experiment, limited to males due to their smallersize, shows that A. anguilla under pressure have a significantly lower oxygen con-sumption than those swimming at the same speed at atmospheric pressure (−40%at 0·5 LT s−1). The results suggest that pressure reduces the cost of swimming byimproving the efficiency of aerobic energy production (Theron et al., 2000) whichappears to be due to a reduction in fluidity of mitochondrial membranes at higherpressures. Indeed, at atmospheric pressure, these membranes become too fluid afterthe silvering process to ensure optimal functioning, which is obtained only when thefish is submitted to increased pressure (Sebert et al., 2009b). This suggests that theoptimal environment, for male silver A. anguilla at least, is at great and constantdepth.

THE LOCATION OF SPAWNING AREAS: WHERE AND WHY?

Spawning areas have only been established with certainty for very few species,mainly on the basis of larval distribution (but, in the case of the A. japonica andA. marmorata, also on the basis of the occurrence of spawning adults). The loca-tion of spawning areas for some species, such as A. dieffenbacchii and Anguillaaustralis Richardson 1841, has been postulated from larval drift patterns (Jellyman& Bowen, 2009). For these species for which something is known, spawning areasare in oligotrophic tropical oceanic regions, typically where water depth exceeds1000 m, generally in frontal zones within the path of warm surface currents (Fig. 2).In the case of the A. japonica, it has been suggested that spawning geography isdetermined by seamounts that are coincident with the right hydrographic conditionsfor larval survival (Tsukamoto et al., 2011), while the A. anguilla and A. rostrataspawn in a general areas bounded by thermal gradients (Kleckner & McCleave, 1985,1988; Tesch & Wegner, 1990). The seamount strategy could provide the fishes withstrong geographic and geomagnetic cues for congregating in given areas, althougha rigid adherence to such cues would preclude the ability of Anguilla spp. to adaptto changing sea conditions; such ecological flexibility has already been suggested asone of the reasons that Anguilla spp. are so widely distributed and are found in awide variety of different habitats (Helfman et al., 1987). While it would appear thattropical Anguilla spp. can spawn all year round (Jellyman, 2003) and possibly in sev-eral locations, e.g. A. marmorata (Budiawan 1997; Minigeshi et al., 2008), temperate

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110

8

3 4

6 7

2 5 9

Fig. 2. Known or suspected spawning sites for well-studied Anguilla spp.: 1, A. anguilla; 2, A. australis; 3, A.bengalensis; 4, A. celebesensis; 5, A. dieffenbachii ; 6, A. japonica; 7, A. marmorata; 8, A. mossambica;9, A. reinhardtii ; 10, A. rostrata. The coasts of regions colonized by them are shaded grey. Warm currentsthat are likely to carry larval Anguilla spp. from spawning areas to the growth habitat are shown byarrows.

Anguilla spp. appear to depend on a single spawning area and a limited spawningseason. This has been established by large-scale field surveys (Schmidt, 1922, forA. anguilla and A. rostrata; Tsukamoto et al., 2011, for A. japonica), but also bythe results of genetic studies that have established that A. rostrata, A. anguilla andA. japonica populations appear to be panmictic (i.e. are a single, mixed population),despite their wide distribution (Tesch, 2003; Wirth & Bernatchez, 2003; Dannewitzet al., 2005; Han et al., 2010; Als et al., 2011). Thus, temperate species (A. anguilla,A. rostrata, A. japonica, A. australis and A. dieffenbachii ) travel at least 2000 km,but possibly up to 9000 km, to a single spawning site. This presents a number ofchallenges, such as the synchronicity of arrival, the difficulties of accurate naviga-tion and maintaining body condition. Nonetheless, the annual arrival at the coasts oflarval and glass Anguilla spp. is proof enough that these challenges are overcome.

The evolution of the long-distance migratory loop is thought to date back to theemergence of the anguillids between 70 and 40 million years ago from a marineancestor (Tsukamoto et al., 2002; Inoue et al., 2010). The emergence of the anguil-lid lineage, which is unique amongst Anguilliformes in occupying fresh water, waspossibly triggered by the opportunity to exploit the relatively risk-free and productivefresh water habitats available in the tropics. Thus, the pattern of spawning at sea, thelarvae drifting back to the coast on ocean currents, and colonization of freshwateris an innate character of the Anguilla genus (Aoyama, 2009). Initially, this trait wasrestricted to species that spawned and colonized tropical habitats but, over time, asland masses shifted, and with the catadromous strategy now deeply ingrained, theevolution of a long distance migratory loop in some species was inevitable. Theextreme long-distance migration observed for today’s temperate Anguilla spp. issimply a consequence of (1) the retention of tropical spawning areas coupled with(2) the evolution of slower growing larvae that enables the colonization of more

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distant growth habitat in temperate areas (Aoyama, 2009). The trade-off that temper-ate species have made in occupying this niche is that conditions for the successfulrecruitment of juveniles are restricted to a few months of the year.

A LEAF BLOWING IN THE WIND? MIGRATION OF LEPTOCEPHALI

It was only with Grassi’s (1896) discovery that Leptocephalus brevirostris was, infact, the larval form of the A. anguilla, that Schmidt (1912) was able to track lepto-cephali of ever decreasing size back to the Sargasso Sea and identify the spawningarea. While this solved one mystery, it revealed another: how did these fragile, glassycreatures manage to travel over thousands of km to the continental shelf? Fisheriesecologists were used to the idea of drifting larvae in shelf seas that, by chance, wouldavoid mortality for long enough to recruit to nursery grounds (Cushing, 1995). Butthe concept of larval fishes that could travel thousands of km on a directed migrationwas something quite different.

Unfortunately, Anguilla spp. leptocephali, by nature of their oceanic existence,are rarely encountered in scientific surveys and, for some species, have not evenbeen discovered. What is known of the lives of leptocephali is slowly being piecedtogether and, by combining information from a number of species, can provideinsights into larval ecology (Miller, 2009). To start, the elopomorph body form andneutrally buoyant gelatinous structure of leptocephali appear to be ideal adaptationsto a life adrift on ocean currents, feeding opportunistically on plankton and fooddebris (Miller, 2009; Tsukamoto, 2009). Their habitat is the near-surface of theocean, between 50 and 400 m. It is without question that the leaf-like shape of theleptocephali is thought to increase the effectiveness of oceanic drift but recent successin rearing leptocephali of A. japonica has enabled direct observation of the swimmingbehaviour and, like adults, it is anguilliform and bi-directional (Miller, 2009; pers.obs.). The extent to which leptocephali can swim for long periods in the manner ofsilver Anguilla spp. is virtually unknown but, nonetheless, Anguilla spp. leptocephaliclearly undertake long migrations between spawning areas and their growth habitat(Fig. 2). The extent to which these migrations are facilitated by oceanic drift, directedswimming, or both remains to be determined (McCleave et al., 1998). On the basisof the fact that leptocephali appear to spend much of their time in depths between 50and 300 m, and therefore significantly deeper than the wind-driven surface currents,it is likely that orientation and directed swimming are important factors in getting thelarval Anguilla spp. to their destination (Bonhommeau et al., 2009, 2010). Indeed,modelling studies have shown that, if leptocephali were just passive travellers onocean currents, it is highly unlikely that they would arrive at continental coastlines(for A. dieffenbachii, Jellyman & Bowen, 2009), either because they would passby landmasses, or become entrained into currents that take them away from theireventual destination (e.g. A. japonica travel in the Kuroshio, and avoid the Mindanao;Miller, 2009). How naïve larvae achieve this migratory feat is unknown.

It is not just the navigation of ocean distances by Anguilla spp. larvae that remainunknown; the duration of larval migrations is also contentious. Recent modellingstudies have suggested that, for the A. anguilla, the oceanic migration can be achievedrelatively quickly, within 1 year (Bonhommeau et al., 2009), provided the lepto-cephali make vertical migrations between near-surface currents to make best use of

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oceanic current systems. By contrast, other authors suggest that patterns of larvaldistribution are more consistent with passive drift and, again for the A. anguilla, ismore likely to take 2–3 years (Kettle & Haines, 2006). Studies have been undertakenwith otoliths to validate these models (Arai et al., 2000; Martin et al., 2010), withvarying levels of success; agreement can be found for both short and long-durationleptocephali migrations. Continued controversy about how to interpret the notionaldaily growth rings in the otoliths of glass eels, however, undermines this validationtechnique (McCleave et al., 1998; Martin el al., 2010), and it seems unlikely thatthis debate will be resolved in the near future. Nonetheless, for now at least, larvalAnguilla spp. have possibly the longest and most extreme migrations of all fish larvae.

THE DECLINE OF ANGUILLA SPP.: MIGHT IT BE A FAILUREOF MIGRATION?

From the preceding sections it can be seen that Anguilla spp. have a range ofunique life-history traits that, judging from their distribution and ubiquity, haveserved them well for millions of years. In the last 40 years, however, all temperatespecies of Anguilla spp. have declined significantly (Casselman & Cairns, 2003),while concerns have begun to be expressed about tropical Anguilla spp. due todisplacement of effort to these stocks. There does not appear to be a single causeof the declines; the reasons cited for stock declines are given variously as climatechange, overfishing, habitat loss or degradation, barriers to migration, or disease orpollution (ICES, 2010). Even attempts to bolster populations by restocking riversor lakes with glass eels may not, according to some, be having the desired effect.Thus, while populations have survived ice ages and have adapted to continental drift(Aoyama, 2009), they may be vulnerable to the rapidity of recent and considerableanthropogenic change to the environment and Anguilla spp. populations (Kettle et al.,2008; Kettle et al., 2010).

Research into the factors that may be influencing the ability of temperate Anguillaspp. stocks to sustain themselves is relatively recent, and much has focused on theeffects of fishing and how to control this (ICES/EIFAC, 2011), particularly in Europe.These efforts, specifically in relation to determining allowable catches or suggest-ing habitat restoration, rely in part on assumptions about the success of Anguillaspp. migrations, either in terms of the success of silver Anguilla spp. in reachingthe spawning areas or in terms of the numbers of larvae that will result from eachspawning event. Recent results from laboratory experiments and analysis, and frommodelling studies, suggest that the migratory capacity of the A. anguilla may becompromised by environmental and biological factors. For example, in tests of swim-ming ability and endurance, Palstra & van den Thillart (2010) showed that A. anguillainfected with the swimbladder parasite Anguillicolloides crassus are unable to sustainswimming for long periods and become exhausted at swimming speeds that, for unin-fected fish, are sustainable for months at a time (van Ginneken et al., 2005a). Theparasite has become endemic in Europe in the last 30 years and A. anguilla in manycatchments across Europe carry high loads of the parasite (Kirk, 2003). The eelvirus European X (EVEX) disease, a naturally occurring virus, also compromisesmigratory performance, with infected fish suffering haemorrhage and mortality quiteearly in simulated migrations, while uninfected controls went on to complete their5500 km swim (van Ginneken et al., 2005b).

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The long-life of temperate Anguilla spp., and their high fat content, is a funda-mental aspect of their adaptation to the long spawning migration, but it is also anAchilles heel in that it makes them vulnerable to the accumulation of lipid solublepollutants. In a study where Anguilla spp. were made to swim a simulated migra-tion, van Ginneken et al. (2009) showed that poly-chlorinated biphenyls (PCB), acommonly occurring pollutant that accumulates in fat deposits of long-lived species,compromise the energy stores available for production of gonad tissue, both in termsof fat quality and fat content. Separately, Palstra et al. (2006) showed that evenlow levels of PCBs increase the mortality of fertilized oocytes. Notwithstanding theeffects of pollutants or disease, Belpaire et al. (2009) have shown that, over the last15 years, the fat content of yellow A. anguilla has fallen by a third in the Nether-lands with the consequence that only the very largest fish would have enough energyreserves left over after the spawning migration to convert to gametes, let alone withhigh quality (high lipid content).

While almost nothing is known about the extent to which pollutants and diseasewere a problem for A. anguilla before the decline in population was identified, theconvergence between the apparent decline in average fish quality and populationdecline due to overfishing and habitat loss may be leading to a precipitous decline(Wirth & Bernatchez, 2003) in the number of successfully spawning fish. Evenassuming that A. anguilla spawn successfully and in large numbers, doubts havesurfaced that there is, any longer, sufficient food for larvae to endure their migration(Bonhommeau et al., 2008) as a result of large-scale, climate driven changes inproductivity in the spawning area. Changing current patterns and multi-decadal trendsin ocean circulation may also be a strong influence on the mortality and migrationsuccess of A. anguilla larvae (Knights 2003; Munk et al., 2010). Similar conditionsand challenges are also facing the A. rostrata (Wirth & Bernatchez, 2003) and A.japonica (Bonhommeau et al., 2008).

OPPORTUNITIES AND CHALLENGES IN ANGUILLA SPP. MIGRATIONRESEARCH

The last 100 years of eel research, starting with the startling and inspirationalinsight of Schmidt (1912) that A. anguilla spawned far away from Europe in theAtlantic Ocean, might be viewed as the beginning of the end to the enduring mysteryof anguillid migrations. Recent decades have resulted in considerable advances inthe understanding of the processes involved in both adult and larval marine migra-tions of freshwater Anguilla spp. There are still unresolved issues, however, that,with every new insight, seem to grow more and not less numerous. Here, some keyareas are listed that will, no doubt, provide an enduring challenge to Anguilla spp.biologists in the future.

I D E N T I F Y I N G T H E S PAW N I N G A R E A S O F A L L A N G U I L L AS P P. , A N D R E F I N I N G T H E U N D E R S TA N D I N G O F K N OW NS PAW N I N G A R E A S

For example, the spawning areas of only four species (A. anguilla, A. rostrata,A, japonica, and Anguilla celebesensis Kaup 1856) are known with any certainty. The

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use of oceanic-flow simulation models (Jellyman & Bowen, 2009) should be infor-mative of possible spawning areas and help to identify areas for future investigationby oceanic larval collections (Tsukamoto et al., 2011).

O B S E RV I N G T H E B E H AV I O U R O F S PAW N I N G A N G U I L L A S P P.

To date, only a handful of Anguilla spp. have ever been caught at a spawningarea (Tsukamoto et al., 2011), despite concerted efforts over the past 100 years.Recent data from electronic tags and from these surveys provide some evidencefor the timing of spawning and the duration of the spawning migration, while thephototaxis observed in some datasets hint at spawning synchronicity with moonphases (Tsukamoto et al., 2011). Nothing is yet known, however, about whetherspawning occurs in large aggregations or in pairs, whether Anguilla spp. spawn inbatches or only once, whether there are multiple spawning sites within a generalspawning area, or if spawning occurs over an extended period.

I D E N T I F Y I N G T H E NAV I G AT I O N M E C H A N I S M ST H AT A N G U I L L A S P P. U S E D U R I N G T H E I R O C E A N I CM I G R AT I O N S

Navigation of highly migratory animals is an area of rich discovery and of somecontroversy. Even for species that are relatively easy to study, such as pigeons,there is still considerable debate about whether navigation is enabled by geomag-netism, a sun compass or visual pilotage (Biro et al., 2004). For species as enigmaticand difficult to study as Anguilla spp., identification of the navigation mechanismis much harder. Recent evidence strengthens the geomagnetic hypothesis for silverA. anguilla (Moore & Riley, 2009), but other hypotheses, such as the imprintinghypothesis (Westin, 1990), which states that A. anguilla trace their way back to thespawning area from cues imprinted on them during the larval migration, have notbeen refuted. Furthermore, evidence from electronic tags suggests that A. anguillaare highly responsive to light levels and time their ascents and descents to dusk anddawn (Aarestrup et al., 2009), raising the possibility that Anguilla spp. may evenuse light to navigate, despite the great depths that they migrate at. Nothing is knownabout the migratory cues used by leptocephali, while glass eels are known to useboth olfactory and tidal cues to find estuaries and to migrate upriver. It is possiblethat Anguilla spp. use multiple cues that operate at different scales and at differ-ent stages in their lifecycle, but this is clearly an area in which much progress isstill to be made. It seems likely that behavioural modelling approaches, combinedwith large-scale ocean models [such as those of Bonhommeau et al. (2008) or Kettle& Haines, (2006)], offer an ideal opportunity for testing hypotheses and narrowingdown areas for more specific experiments.

H OW U N D E R S TA N D I N G A N G U I L L A S P P. M I G R AT I O N S M I G H TH E L P AQ UAC U LT U R E

As for any fish species that has a commercial market, especially species that arein decline, the prospect of gaining independence from the fluctuations in wild stockby developing aquaculture is attractive. Anguilla spp. are, of course, farmed acrossthe world, but this farming procedure is more accurately described as on-growing.

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The production of spawners is a very intensive process, made possible only bythe regular injection of hormones. Furthermore, the mortality of eggs and larvae isvery high (Okamura et al., 2011), and therefore culturing Anguilla spp. from thefull life-cycle is not yet economically feasible. From tagging experiments and trialsin aquaculture facilities, however, many of the conditions that are prerequisite forAnguilla spp. maturation during the spawning migration are now relatively wellknown. For example, daily temperature cycling is a feature of the migrations offemale A. japonica, A. anguilla and A. dieffenbachii eel. In recent experiments,A. japonica matured under constant temperature conditions showed poorer conditionthan those matured under a thermal cycle (Sudo et al., 2011).

Holding Anguilla spp. under differing pressure cycles is technically difficult, butsince pressure can alter biological processes through the modifications of enzymekinetics and membrane structure, composition and fluidity, both of which are impor-tant in egg development, this may be a productive area for research. Lots of theadaptations developed in silver Anguilla spp. suggest that reproductive acts (ovula-tion, spermination and egg fertilization) take place at great depth.

Finally, swimming exercise is also known to promote maturation in A. anguillaeels (Palstra et al., 2007, 2009; Palstra & van den Thillart, 2010; Palstra & Planas,2011). Knowledge of swimming efficiency and endurance will enable selection of thebest broodstock, but also help to define husbandry procedures that will ensure thatAnguilla spp. can be in the best possible condition before and during the maturationprocess, thereby maximizing production of eel larvae. In turn, a better understandingof the behaviour of larvae and their preferred diets might make it possible to compressappreciably the long larval life of Anguilla spp., and increase the (currently) verysmall proportion of larvae that survive to the glass eel stage.

I N T E G R AT I N G K N OW L E D G E O F A N G U I L L A S P P. M I G R AT I O NI N T O M A NAG E M E N T P L A N S

The concerns expressed over the status of temperate Anguilla spp. populations,and the potential for displacement of fishing effort to tropical species mean thatintegrating any relevant knowledge is a priority. In the case of Anguilla spp. migra-tions or migration success, there are factors that cannot be controlled, such as globalclimate and productivity of oceans or rivers, and factors that are difficult to control,such as fishing, barriers to migration and pollution. While modelling Anguilla spp.population dynamics is very difficult because of the complexities of life-history (e.g.mixed cohort spawning and lack of a stock–recruitment relationship), knowledge ofAnguilla spp. migrations, such as mortality or disorientation in the downriver phase(Aarestrup et al., 2008; Westerberg & Lagenfelt, 2008), the probability of successin reaching the spawning area (Aarestrup et al., 2009), the breeding condition andfecundity of migrating females (Dufour & van den Thillart, 2009), or the proportionof larvae that successfully migrate to the continental growth habitat (Bonhommeauet al., 2008), can all help to increase the success in identifying appropriate targetsfor anthropogenic mortality of Anguilla spp. at the glass, yellow or silver phase(ICES, 2010).

This paper was written with the support of funding from Grant Agreement GOCE-2008212133 (EELIAD) of the European Union FP7 research programme on Environment(including climate change), as part of a collaboration between the authors that extended from

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the ‘FitFish Symposium’ in Barcelona in July 2010, through the ‘Eel Expo’ in Tokyo inJuly 2011, concluding in the ‘Anguillid eel session’ at the 6th World Fisheries Congress inEdinburgh in May 2012.

References

Aarestrup, K., Thorstad, E. B., Koed, A., Jepsen, N., Svendsen, J. C., Pedersen, M. I., Skov, C.& Økland, F. (2008). Survival and behaviour of European silver eels in late freshwaterand early marine phase during spring migration. Fisheries Management and Ecology15, 435–440.

Aarestrup, K., Økland, F., Hansen, M. M., Righton, D., Gargan, P., Castonguay, M.,Bernatchez, L., Howey, P., Sparholt, H., Pedersen, M. I. & McKinley, R. S. (2009).First empirical results on the ocean spawning migrations of the European eel (Anguillaanguilla). Science 325, 1660.

Als, T. D., Hansen, M. M., Maes, G. E., Castonguay, M., Riemann, L., Aarestrup, K., Munk,P., Sparholt, H., Hanel, R. & Bernatchez, L. (2011). All roads lead to home: panmixiaof European eel in the Sargasso Sea. Molecular Ecology 20, 1333–1346.

Aoyama, J. (2009). Life history and evolution of migration in catadromous eels (genusAnguilla). Aquatic Bio-science Monographs 2, 1–42.

Aoyama, J., Hissmann, K., Yoshinaga, T., Sasai, S., Uto, T. & Ueda, H. (1999). Swimmingdepth of migrating silver eels Anguilla japonica released at seamounts of the westMariana Ridge, their estimated spawning sites. Marine Ecology Progress Series 186,265–269.

Arai, T., Otake, T. & Tsukamoto, K. (2000). Timing of metamorphosis and larval segre-gation of the Atlantic eels Anguilla rostrata and A. anguilla, as revealed by otolithmicrostructure and microchemistry. Marine Biology 137, 39–45.

Aroua, S., Schmitz, M., Baloche, S., Vidal, B., Rosseau, K. & Dufour, S. (2005). Endocrineevidence that silvering, a secondary metamorphosis in the eel, is a pubertal rather thana metamorphic event. Neuroendocrinology 8, 221–232.

Avise, J. C., Helfman, G. S., Saunders, N. C. & Hales, L. S. (1986). Mitochondrial DNA dif-ferentiation in North Atlantic eels: population genetics consequences of an unusual lifehistory pattern. Proceedings of the National Academy of Science of the United States ofAmerica 83, 4350–4354.

Avise, J. C., Nelson, W. S., Arnold, J., Koehn, R. K., Williams, G. C. & Thorsteinsson, V.(1990). The evolutionary genetic status of Icelandic eels. Evolution 44, 1254–1262.

Baras, E. & Jeandrain, D. (1998). Evaluation of surgery procedures for tagging eel Anguillaanguilla (L.) with biotelemetry transmitters. Hydrobiologia 371/372, 107–111.

Belpaire, C. G. J., Goemans, G., Geeraerts, C., Quataert, P., Parmentier, K., Hagel, P. &Boer, J. D. (2009). Decreasing eel stocks: survival of the fattest? Ecology of FreshwaterFish 18, 197–214.

Biro, D., Meade, J. & Guilford, T. (2004). Familiar route loyalty implies visual pilotagein the homing pigeon. Proceedings of the National Academy of Sciences 101,17440–17443.

Boetius, I. & Boetius, J. (1967). Eels. Anguilla rostrata LeSeuer, in Bermuda. VidenskabeligeMeddelelser Dansk Naturhistorisk Forening 150, 65–84.

Bone, Q., Marshall, N. B. & Blaxter, J. H. (1995). Biology of Fishes. London: Chapman &Hall.

Bonhommeau, S., Chassot, E., Planque, B., Rivot, E., Knap, A. H. & Le Pape, O. (2008).Impact of climate on eel populations of the Northern Hemisphere. Marine EcologyProgress Series 373, 71–80.

Bonhommeau, S., Le Pape, O., Gascuel, D., Blanke, B., Treguier, A.-M., Grima, N., Vermard,Y., Castonguay, M. & Rivot, E. (2009). Estimates of the mortality and the durationof the trans-Atlantic migration of European eel Anguilla anguilla leptocephali using aparticle tracking model. Journal of Fish Biology 74, 1891–1914. doi: 10.1111/j.1095-8649.2009.02298.x

© 2012 Crown CopyrightJournal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, 81, 365–386

382 D . R I G H T O N E T A L .

Bonhommeau, S., Castonguay, M., Rivot, E., Sabatie, R. & Le Pape, O. (2010). The dura-tion of migration of Atlantic Anguilla larvae. Fish and Fisheries 11, 289–306. doi:10.1111/j.1467-2979.2010.00362.x

Burgerhout, E., Manabe, R., Brittijn, S. A., Aoyama, J., Tsukamoto, K. & van den Thillart,G. E. E. J. M. (2011). Dramatic effect of pop-up satellite tags on eel swimming. Natur-wissenschaften 98, 631–634.

Casselman, J. & Cairns, D. (2003). Worldwide decline of eel resources necessitates immediateaction: Quebec declaration of concern. Fisheries 28, 28–30.

Chow, S., Kurogi, H., Katayama, S., Ambe, D., Okazaki, M., Watanabe, T., Ichikawa, T.,Kodama, M., Aoyama, J., Shinoda, A., Watanabe, S., Tsukamoto, K., Miyazaki, S.,Kimura, S., Yamada, Y., Nomura, K., Tanaka, H., Kazeto, Y., Hata, K., Handa, T.,Tawa, A. & Mochioka, N. (2010). Japanese eel Anguilla japonica do not assimilatenutrition during the oceanic spawning migration: evidence from stable isotope analysis.Marine Ecology Progress Series 402, 233–238.

Comparini, A. & Rodino, E. (1980). Electrophoretic evidence for two species of Anguillaleptocephali in the Sargasso Sea. Nature 287, 435–437.

Cushing, D. (1995). Population Production and Regulation in the Sea: A Fisheries Perspective.Cambridge: Cambridge University Press.

Dannewitz, J., Maes, G. E., Johansson, L., Wickstrom, H., Volckaert, F. A. M. & Torbjorn,J. (2005). Panmixia in the European eel: a matter of time. Proceedings of the RoyalSociety B 272, 1129–1137.

Dekker, W. (2003). Status of the European eel stock and fisheries. In Eel Biology (Aida, K.,Tsukamoto, K. & Yamauchi, K., eds), pp. 237–254. Tokyo: Springer-Verlag.

Dufour, S. & van den Thillart, G. (2009). Reproduction capacity of European eels. In SpawingMigration of the European Eel (van den Thillart, G., Dufour, S. & Rankin, C., eds),pp. 465–473. Berlin: Springer.

Fort, T. (2003). The Book of Eels. London: Harper Collins.Fricke, H. & Kaese, R. (1995). Tracking of artificially matured eels (Anguilla anguilla) in

the Sargasso Sea and the problem of the eel’s spawning site. Naturwissenschaften 82,32–36.

van Ginneken, V. & Maes, G. E. (2005). The European eel (Anguilla anguilla, Linnaeus), itslifecycle, evolution and reproduction: a literature review. Reviews in Fish Biology andFisheries 15, 367–398.

van Ginneken, V. & van den Thillart, G. (2000). Eel fat stores are enough to reach theSargasso. Nature 403, 156–157.

van Ginneken, V., Antonissen, E., Muller, U., Booms, R., Eding, E., Verreth, J. & van denThillart, G. (2005a). Eel migration to the Sargasso: remarkably high swimming effi-ciency and low energy costs. Journal of Experimental Biology 208, 1329–1335.

van Ginneken, V., Ballieux, B., Willemze, R., Coldenhoff, K., Lentjes, E., Antonissen, E.,Haenen, O. & van den Thillart, G. (2005b). Hematology patterns of migrating Euro-pean eels and the role of EVEX virus. Comparative Biochemistry and Physiology C140, 97–102.

van Ginneken, V., Palstra, A., Leonards, P., Nieveen, M., Van Den Berg, H., Flik, G., Span-ings, T., Niemantsverdriet, P., van den Thillart, G. & Murk, A. (2009). PCBs and theenergy cost of migration in the European eel (Anguilla anguilla L.). Aquatic Toxicology92, 213–220.

Grassi, G. B. (1896). The reproduction and metamorphosis of the common eel (Anguillavulgaris). Proceedings of the Royal Society 60, 260–271. doi: 10.1098/rspl.1896.0045

Han, Y. S., Hung, C. L., Liao, Y. F. & Tzeng, W. N. (2010). Population genetic structure ofthe Japanese eel Anguilla japonica: panmixia at spatial and temporal scales. MarineEcology Progress Series 401, 221–232.

Haro, A. J. (1991). Thermal preferenda and behavior of Atlantic eels (genus Anguilla) inrelation to their spawning migration. Environmental Biology of Fish 31, 171–184.

Helfman, G. S., Facey, D. J., Hales, J. L. S. & Bozeman, J. E. L. (1987). Reproductive ecol-ogy of the American eel. American Fisheries Society Symposium 1, 42–56.

Inoue, J. G., Miya, M., Miller, M. J., Sado, T., Hanel, R., Hatooka, K., Aoyama, J., Minegishi,Y., Nishida, M. & Tsukamoto, K. (2010). Deep-ocean origin of the freshwater eels.Biology Letters 6, 363–366. doi: 10.1098/rsbl.2009.0989

© 2012 Crown CopyrightJournal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, 81, 365–386

T H E A N G U I L L A S P P. M I G R AT I O N P RO B L E M 383

Jellyman, D. J. (2003). The distribution and biology of the South Pacific species of Anguilla .In Eel Biology (Aida, K., Tsukamoto, K. & Yamakchi, K., eds), pp. 275–292. Tokyo:Springer.

Jellyman, D. J. & Bowen, M. M. (2009). Modeling larval migration routes and spawningareas of anguillid eels of Australia and New Zealand. American Fisheries SocietySymposium 69, 255–274.

Jellyman, D. J. & Lambert, P. W. (2003). Factors affecting recruitment of glass eels into theGrey River, New Zealand. Journal of Fish Biology 63, 1067–1079. doi: 10.1046/j.1095-8649.2003.00220.x

Jellyman, D. & Tsukamoto, K. (2002). First use of archival transmitters to track migratingfreshwater eels Anguilla dieffenbachii at sea. Marine Ecology Progress Series 233,207–215.

Jellyman, D. & Tsukamoto, K. (2005). Swimming depths of offshore migrating longfin eelsAnguilla dieffenbachii. Marine Ecology Progress Series 286, 261–267.

Jellyman, D. J. & Tsukamoto, K. (2010). Vertical migrations may control maturation inmigrating female Anguilla dieffenbachii. Marine Ecology Progress Series 404,241–247.

Jellyman, D. J., Booker, D. J. & Watene, E. (2009). Recruitment of Anguilla spp. glass eelsin the Waikato River, New Zealand. Evidence of declining migrations? Journal of FishBiology 74, 2014–2033. doi: 10.1111/j.1095-8649.2009.02241.x

Kettle, A. & Haines, K. (2006). How does the European eel (Anguilla anguilla) retain its pop-ulation structure during its larval migration across the North Atlantic Ocean? CanadianJournal of Fisheries and Aquatic Sciences 63, 90–106.

Keltle, A. J., Bakker, D. C. E. & Haines, K. (2008). Impact of the North Atlantic Oscilationon the trans. Atlantic migrations of the European eel (Anguilla anguilla). Journal ofGeophysical Research 113, G03004. doi: 10.1029/2007JG000589

Kettle, A. J., Asbjørn Vøllestad, L. & Wibig, J. (2011). Where once the eel and the elephantwere together: decline of the European eel because of changing hydrology in southwestEurope and northwest Africa? Fish and Fisheries 12, 380–411. doi: 10.1111/j.1467-2979.2010.00400.x.

Kirk, R. S. (2003). The impact of Anguillicola crassus on European eels. Fisheries Manage-ment and Ecology 10, 385–394.

Kleckner, R. C. (1980). Swimbladder volume maintenance related to initial migratory depthin silverphase Anguilla rostrata. Science 208, 1481–1482.

Kleckner, R. C. & Krueger, W. H. (1981). Changes in swimbladder retial morphology inAnguilla rostrata during premigration metamorphosis. Journal of Fish Biology 18,569–577.

Kleckner, R. C. & McCleave, J. D. (1985). Spatial and temporal distribution of American eellarvae in relation to North Atlantic Ocean current systems. Dana 4, 67–92.

Kleckner, R. C. & McCleave, J. D. (1988). The northern limit of spawning by Atlantic eels(Anguilla spp.) in the Sargasso Sea in relation to thermal fronts and surface watermasses. Journal of Marine Research 46, 647–667.

Knights, B. (2003). A review of the possible impacts of long-term oceanic and climate changesand fishing mortality on recruitment of anguillid eels of the Northern Hemisphere. TheScience of the Total Environment 310, 237–244.

Manabe, R., Aoyama, J., Watanabe, K., Kawai, M., Miller, M. J. & Tsukamoto, K. (2011).First observations of the oceanic migration of Japanese eel, from pop-up archivaltransmitting tags. Marine Ecology Progress Series 437, 229–240.

Martin, J., Daverat, F., Pecheyran, C., Als, T. D., Feunteun, E. & Reveillac, E. (2010). Anotolith microchemistry study of possible relationships between the origins of lepto-cephali of European eels in the Sargasso Sea and the continental destinations andrelative migration success of glass eels. Ecology of Freshwater Fish 19, 627–637. doi:10.1111/j.1600-0633.2010.00444.x

McCleave, J. D. (1980). Swimming performance of European eel (Anguilla anguilla L.)elvers. Journal of Fish Biology 16, 445–452.

McCleave, J. D. & Arnold, G. P. (1999). Movements of yellow- and silver-phase Europeaneels (Anguilla anguilla L.) tracked in the western North Sea. ICES Journal of MarineScience 56, 510–536.

© 2012 Crown CopyrightJournal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, 81, 365–386

384 D . R I G H T O N E T A L .

McCleave, J. D. & Kleckner, R. C. (1982). Selective tidal stream transport in the estuarinemigration of glass eels of the American eel (Anguilla rostrata). Journal du Conseilinternational pour l’Exploration de la Mer 40, 262–271.

McCleave, J. D. & Stred, K. A. (1975). Effect of dummy telemetry transmitters on staminaof Atlantic salmon (Salmo salar) smolts. Journal of the Fisheries Research Board ofCanada 32, 559–563.

McCleave, J. D., Brickley, P. J., O’Brien, K. M., Kistner-Morris, D. A., Wong, M. W., Gal-lagher, M. & Watson, S. M. (1998). Do leptocephali of the European eel swim to reachcontinental waters? Status of the question. Journal of the Marine Biological Associationof the United Kingdom 78, 285–306.

Methling, C., Tudorache, C., Skov, P. V. & Steffensen, J. F. (2011). Pop up satellite tagsimpair swimming performance and energetics of the European eel (Anguilla anguilla).PLoS One 6, e20797. doi:10.1371/journal.pone.0020797

Miller, M. (2009). Ecology of anguilliform leptocephali: remarkable transparent fish larvaeof the ocean surface layer. Aquatic-Biosciences Monographs 4, 1–94.

Minegishi, Y., Aoyama, J. & Tsukamoto, K. (2008). Multiple population structure of the giantmottled eel Anguilla marmorata. Molecular Ecology 17, 3109–3122.

Moore, A. R. & Riley, W. D. (2009). Magnetic particles associated with the lateral line ofthe European eel Anguilla anguilla. Journal of Fish Biology 74, 1629–1634.

Munk, P., Hansen, M. M., Maes, G. E., Nielsen, T. G., Castonguay, M., Riemann, L., Sparholt,H., Als, T. D., Aarestrup, K., Andersen, N. G. & Bachler, M. (2010). Oceanic frontsin the Sargasso Sea control the early life and drift of Atlantic eels. Proceedings of theRoyal Society B 277, 3593–3599.

Nieddu, M., Pichiri, G., Coni, P., Salvadori, S., Deiana, A. M. & Mezzanotte, R. (1998). Acomparative analysis of European and American eel (Anguilla anguilla and Anguillarostrata) genomic DNA: 5S rDNA polymorphism permits the distinction between thetwo populations. Genome 41, 728–732.

Nilsson, L., Nyman, L., Westin, L. & Ornhagen, H. (1981). Simulation of the reproduc-tive migration of european eels (Anguilla anguilla, L.) through manipulation of someenvironmental factors under hydrostatic compression. Speculations in Science and Tech-nology 4, 475–484.

Okamura, A., Yamada, Y., Mikawa, N., Horie, N., Tanaka, S. & Tsukamoto, K. (2011). Noto-chord deformities in reared Japanese eel Anguilla japonica larvae, Aquaculture 317,37–41. doi: 10.1016/j.aquaculture.2011.04.024

Palstra, A. P. & Planas, J. V. (2011). Fish under exercise. Fish Physiology and Biochemistry37, 259–272.

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 reproduc-tion. Fish Physiology and Biochemistry 36, 297–322. doi: 10/1007/S10695-010-9397-4

Palstra, A. P., Van Ginneken, V. J. T., Murk, A. J. & van den Thillart, G. E. E. J. M. (2006).Are dioxin-like contaminants responsible for the eel (Anguilla anguilla) drama? Natur-wissenschaften 93, 145–148.

Palstra, A., Curiel, D., Fekkes, M., de Bakker, M., Szekely, C., van Ginneken, V. & vanden Thillart, G. (2007). Swimming stimulates oocyte development in European eel.Aquaculture 270, 321–332.

Palstra, A., van Ginneken, V. & van den Thillart, G. (2008). Cost of transport and opti-mal swimming speed in farmed and wild European silver eels (Anguilla anguilla).Comparative Biochemistry and Physiology A 151, 37–44.

Palstra, A., van Ginneken, V. & van de Thillart, G. (2009). Effects of swimming on silveringand maturation of the European eel, Anguilla anguilla L. In Spawning Migration ofthe European Eel (van den Thillart, G., Dufour, S. Rankin, J. C., eds), pp. 229–251.Berlin: Springer.

Prosek, J. (2010). Eels: An Exploration, from New Zealand to the Sargasso, of the World’sMost Mysterious Fish. London: Harper-Collins.

Quintella, B. R., Mateus, C. S., Costa, J. L., Domingos, I. & Almeida, P. R. (2010). Criticalswimming speed of yellow- and silver- phase European eel (Anguilla anguilla L.).Journal of Applied Ichthyology 26, 432–435.

© 2012 Crown CopyrightJournal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, 81, 365–386

T H E A N G U I L L A S P P. M I G R AT I O N P RO B L E M 385

Rankin, J. C. (2009). Acclimation to sea water in European eel Anguilla anguilla: effects ofsilvering. In Spawning Migration of the European Eel (van den Thillart, G., Dufour, S.,Rankin, J. C., eds), pp. 129–145. Berlin: Springer.

Rousseau, K., Aroua, S., Schmitz, M., Elie, P. & Dufour, S. (2009). Silvering: metamor-phosis or puberty. In Spawning Migration of the European Eel (van den Thillart, G.,Dufour, S., Rankin, J. C., eds), pp. 39–63. Berlin: Springer.

Scaion, D., Belhomme, M. & Sebert, P. (2008). Pressure and temperature interactions onaerobic metabolism of European silver eel. Respiratory Physiology and Neurobiology164, 319–322.

Schmidt, J. (1912). The reproduction and spawning places of the fresh-water eel (Anguillavulgaris) Nature 89, 633–636.

Schmidt, J. (1922). The breeding places of the eel. Philosophical Transactions of the RoyalSociety B 211, 179–208. doi: 10.1098/rstb.1923.0004

Schmidt-Nielsen, K. (1972). Locomotion: energy cost of swimming, flying and running. Sci-ence 177, 222–228.

Sebert, P. (2008). Fish muscle function and pressure. In Fish Life in Some Special Envi-ronments: Physiological Functions (Sebert, P., Onyango, D. & Kapoor, B. G., eds),pp. 233–255. Enfield, NH: Science Publishers.

Sebert, P. & Macdonald, A. G. (1993). Fish. Effects of high pressure on biological systems. InAdvances in Comparative and Environmental Physiology, Vol. 17 (Macdonald, A. E.,ed.), pp. 147–196. Berlin: Springer Verlag.

Sebert, P., Vettier, A. & Belhomme, M. (2004). A simple relationship to calculate eel surfacearea : interest in studying energy metabolism. Animal Biology 54, 131–136.

Sebert, P., Vettier, A., Amerand, A. & Moisan, C. (2009a). High pressure resistance andadaptation of European eels. In Spawning Migration of the European Eel (van denThillart, G., Dufour, S., Rankin, J. C., eds), pp. 99–127. Berlin: Springer.

Sebert, P., Scaion, D. & Belhomme, M. (2009b). High hydrostatic pressure improves theswimming efficiency of European migrating silver eel. Respiratory Physiology andNeurobiology 165, 112–114.

Sudo, R., Tosaka, R., Ijiri, S., Adachi, S., Suetake, H., Suzuki, Y., Horie, N., Tanaka, S.,Aoyama, J. & Tsukamoto, K. (2011). Effect of temperature decrease on oocyte devel-opment, sex steroids, and gonadotropin β-subunit mRNA expression levels in femaleJapanese eel Anguilla japonica. Fisheries Science 77, 575–582. doi: 10.1007/s12562-011-0358-3

Svedang, H. & Wickstrom, H. (1997). Low fat contents in female silver eels: indications ofinsufficient energetic stores for migration and gonadal development. Journal of FishBiology 50, 475–486.

Tagliavini, J., Harrison, I. J. & Gandolfi, G. (1995). Discrimination between Anguilla anguillaand Anguilla rostrata by polymerase chain reaction–restriction fragment length poly-morphism analysis. Journal of Fish Biology 47, 741–743.

Tesch, F-W. (1974). Influence of geomagnetism and salinity on the directional choice of eels.Helgolander Wissenschaftliche Meeresuntersuchungen 26, 382–395.

Tesch, F-W. (1977). The Eel. Biology and Management of Anguillid Eels. London: Chapman& Hall.

Tesch, F-W. (1978). Telemetric observations on the spawning migration of the eel (Anguillaanguilla) west of the European continental shelf. Environmental Biology of Fish 3,203–209.

Tesch, F-W. (1989). Changes in swimming depth and direction of silver eels (Anguillaanguilla L.) from the continental shelf to the deep sea. Aquatic Living Resources2, 9–20.

Tesch, F-W. (1995). Vertical movements of migrating silver eels (Anguilla anguilla) in thesea. Bulletin of Sea Fisheries Institutes 2, 24–30.

Tesch, F-W. (2003). The Eel. Oxford: Blackwell Science .Tesch, F.-W. & Wegner, G. (1990). The distribution of small larvae of Anguilla sp. related

to hydrographic conditions 1981 between Bermuda and Puerto Rico. InternationaleRevue der gesamten Hydrobiologie 75, 845–858.

Tesch, F-W., Westerberg, H. & Karlsson, L. (1991). Tracking studies on migrating silver eelsin the Central Baltic. Meeresuntersuchungen 33, 183–196.

© 2012 Crown CopyrightJournal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, 81, 365–386

386 D . R I G H T O N E T A L .

Theron, M., Guerrero, F. & Sebert, P. (2000). Improvement of oxidative phosphorylationefficiency in the yellow freshwater eel acclimatised to 101 ATA hydrostatic pressure.Journal of Experimental Biology 203, 3019–3023.

van den Thillart, G. & Dufour, S. (2009). How to estimate the reproductive success of Euro-pean silver eels. In Spawning Migration of the European Eel (van den Thillart, G.,Dufour, S. & Rankin, C., eds), pp. 3–9. Berlin: Springer.

van den Thillart, G., van Ginneken, V., Korner, F., Heijmans, R., van der Linden, R. &Gluvers, A. (2004). Endurance swimming of European eel. Journal of Fish Biology65, 312–318.

Todd, P. R. (1980). Size and age of migrating New Zealand freshwater eels (Anguilla spp.).New Zealand Journal of Marine and Freshwater Research 14, 283–293.

Todd, P. R. (1981). Timing and periodicity of migrating New Zealand freshwater eels (Anguillaspp.). New Zealand Journal of Marine and Freshwater Research 15, 225–235.

Tsukamoto, K. (2009). Oceanic migration and spawning of anguillid eels. Journal of FishBiology 74, 1833–1852.

Tsukamoto, K., Aoyama, J. & Miller, M. J. (2002). Migration, speciation and the evolutionof diadromy in anguillid eels. Canadian Journal of Fisheries and Aquatic Science 59,1989–1998.

Tsukamoto, K., Chow, S., Otake, T., Kurogi, H., Mochioka, N., Miller, M. J., Kimura, S.,Watanabe, S., Yoshinaga, T., Shinoda, A., Kuroki, M., Oya, M., Watanabe, T., Hata, K.,Ijiri, S., Kazeto, Y., Nomura, K. & Tanaka, H. (2011). Oceanic spawning ecology offreshwater eels in the western North Pacific. Nature Communications. doi: 10.1038/ncomms1174

Tucker, D. W. (1959). A new solution to the Atlantic eel problem. Nature 183, 495–501.Videler, J. J. (1993). Fish Swimming. London: Chapman & Hall.Verreault, G., Mingelbier, M. & Dumont, P. (2012). Spawning migration of American eel

Anguilla rostrata from pristine (1843–1872) to contemporary (1963–1990) periods inthe St Lawrence River estuary, Canada. Journal of Fish Biology 81, 387–407.

Webb, P. W. (1971). The swimming energetics of trout. 1. Thrust and power at cruisingspeeds. Journal of Experimental Biology 55, 489–520.

Westerberg, H. (1979). Counter-current orientation in the migration of the European eel.Rapports et Proces-verbaux des reunions Conseil international pour l’Exploration dela Mer 174, 134–143.

Westerberg, H. & Lagenfelt, I. (2008). Sub-sea power cables and migration behaviour of theEuropean eel. Fisheries Management and Ecology 15, 369–375.

Westin, L. (1990). Orientation mechanisms in migrating European silver eel (Anguilla an-guilla): temperature and olfaction. Marine Biology 106, 175–179. doi: 10.1007/BF01314798

Williams, G. C. & Koehn, K. (1984). Population genetics of North Atlantic catadromous eels(Anguilla). In Evolutionary Genetics of Fishes (Turner, B. J., ed.), pp. 529–556. NewYork, NY: Plenum Press.

Wirth, T. & Bernatchez, L. (2003). Decline of North Atlantic eels: a fatal synergy? Proceed-ings of the Royal Society B 270, 681–688.

Electronic References

Aristotle (350BC). The History of Animals. Available at http://classics.mit.edu/Aristotle/history_anim.6.vi.html/ (accessed on November 2011).

ICES (2010). Report of the 2010 session of the joint EIFAC/ICES working group on eels.Available at http://www.ices.dk/workinggroups/ViewWorkingGroup.aspx?ID=75/(accessed 1 November, 2011).

ICES/EIFAC (2011). Report of the 2010 session of the Joint EIFAC/ICES Working Group OnEels. EIFAC Occasional Paper No. 47 and ICES CM 2010/ACOM: 18. Rome: FAO andCopenhegen: ICES. Available at www.Ices.dk/reports/ACOM/2010/WGEEL/Wgeel_2010_FAO.pdf

© 2012 Crown CopyrightJournal of Fish Biology © 2012 The Fisheries Society of the British Isles, Journal of Fish Biology 2012, 81, 365–386