Swimming stimulates oocyte development in European eel

In this study, we subjected eels from Lake Balaton (Hungary) to a swimming period of 1 week and 2 or 6 weeks. Most eels were silver and were 13–21 years old. Time dependent changes in morphometrical parameters and developmental characteristics of the oocytes were determined. Already after 1 week of swimming, the gonadal mass increased and oocytes became larger, filled with large numbers of lipid droplets. After 2 and 6 weeks of swimming we found in addition a significant enlargement of the eyes, which is a sign of sexual maturation. In contrast to the resting eels, that had oocytes in the primary growth phase (stage 1–2); the swimming eels had oocytes in stage 3; the cortical alveolus or lipid droplet stage. The results indicate that lipid mobilisation induced by swimming is a requirement for the natural incorporation of lipid droplets in the oocytes, a crucial step in oocyte maturation. As the Balaton eels responded stronger to swimming than young farmed eels, it is suggested that older eels are more sensitive for maturation triggers.     

Swimming physiology of European silver eels (<Emphasis Type="Italic">Anguilla anguilla</Emphasis> L.): energetic costs and effects on sexual maturation and reproduction

The European eel migrates 5,000–6,000 km to the Sargasso Sea to reproduce. Because they venture into the ocean in a pre-pubertal state and reproduce after swimming for months, a strong interaction between swimming and sexual maturation is expected. Many swimming trials have been performed in 22 swim tunnels to elucidate their performance and the impact on maturation. European eels are able to swim long distances at a cost of 10–12 mg fat/km which is 4–6 times more efficient than salmonids. The total energy costs of reproduction correspond to 67% of the fat stores. During long distance swimming, the body composition stays the same showing that energy consumption calculations cannot be based on fat alone but need to be compensated for protein oxidation. The optimal swimming speed is 0.61–0.67 m s⁻¹, which is ~60% higher than the generally assumed cruise speed of 0.4 m s⁻¹ and implies that female eels may reach the Sargasso Sea within 3.5 months instead of the assumed 6 months. Swimming trials showed lipid deposition and oocyte growth, which are the first steps of sexual maturation. To investigate effects of oceanic migration on maturation, we simulated group-wise migration in a large swim-gutter with seawater. These trials showed suppressed gonadotropin expression and vitellogenesis in females, while in contrast continued sexual maturation was observed in silver males. The induction of lipid deposition in the oocytes and the inhibition of vitellogenesis by swimming in females suggest a natural sequence of events quite different from artificial maturation protocols.     

Migration and escapement of silver eel males,Anguilla anguilla,from a southwestern European river

The catadromous life cycle of the European eel encompasses a spawning migration to the Sargasso Sea. Prior to their migration, eels develop a silver coloration being referred to as “silver eels.” Due to the dramatic European eel recruitment decline, it is crucial to quantify silver eel escapement to evaluate the success of measures taken under Eel Management Plans (Regulation EC (1100/2007)). Thus, the percentage of silver eels escaping from the River Mondego (Portugal) was estimated during two consecutive spawning seasons (2014–2016) and their migratory behaviour was studied. Thirty-six male silver eels were tagged with acoustic transmitters and their downstream migration was tracked using automatic receivers deployed at four locations along the river course, from the first impassable obstacle up to the river mouth (67 km). Among the tagged eels, 15 (42%) escaped to the sea. In both years, individuals displayed faster migration speed in the downstream reaches of the river. BRT (“Boosted Regression Trees”) models were used to explain downstream migration and escapement of silver eels. The analyses revealed that the downstream migration is triggered by several environmental variables with water conductivity as the most influential predictor. Escapement of eels from the estuary occurred a few hours after their arrival and was primarily explained by the offshore wind intensity, which promotes a current in the coast that may favour their transport to the open sea. These findings contribute to a better understanding of silver eel migration in southern latitudes and highlight and reinforce the need to monitor spawner escapement.     

Behaviour,escapement and mortality of female European silver eels within a regulated lowland river draining into the Baltic Sea

Migration patterns of 146 female silver eels on their way through fresh and brackish water stretches of the Warnow River into the Baltic Sea were studied using acoustic telemetry. The majority of eels (77%) regained their expected downstream migration behaviour after a median rehabilitation time of 2 days. Positive rheotactic behaviour was observed for 23% of tagged eels after release, probably influenced by experimental procedures. The observed silver eel escapement rate was 63%. Two migratory groups were classified by significantly different migratory speed, time of residence in brackish waters and biometric silvering characteristics. Although the classification of silvering stages is based on these measures, the proportions of these stages did not reflect the observed differences in migratory behaviour. In the context of a permanent silver eel descent in the freshwater part of the Warnow River, a permanent escapement was likewise occurring into the Baltic Sea.     

A preliminary experiment regarding the natural induction of gonadal development in female Japanese eels without hormone treatment

To test whether gonadal development of female eels could be promoted without any exogenous hormone treatments, we observed the effect of water temperature manipulation. After 3–5 months of water temperature treatments, three silver eels showed higher gonadosomatic indices (GSI). In particular, one eel in the 5–15°C fluctuating temperature treatment group (5°C daytime and 15°C night‐time) had the highest GSI of 8.5 with secondary yolk globule stage oocytes of large diameter (OD; 412 μm) after 3 months, which indicated definite gonadal development compared with those in the initial states (mean GSI, 2.4; OD, 226.7 μm). The 5–15°C fluctuating temperature and constant 5°C groups had low oocyte breakdown (atretic) rates. Because daily temperature fluctuations and cold daytime water are experienced by vertically migrating silver eels in the ocean, these temperature conditions may be key maturation process components that could be useful for hormone‐free artificial maturation.     

A preliminary telemetry study of the migration of silver European eel (Anguilla anguilla L.) in the River Mosel, Germany

Abstract  – To study the behaviour of silver eels ( Anguilla anguilla L.) during their downstream migration, particularly near a hydroelectric power dam, we tagged nine eels with ultrasonic transmitters and tracked their paths in the River Mosel, Germany. The onset of migration coincided with the first flood event that followed the full moon but was independent of daytime, because migration and turbine passage occurred during both day and night. During migration eels swam actively downstream with a velocity of 0.3–1.2 m · s⁻¹. When migrating eels arrived at the dam, they either passed through the turbines immediately or stayed upstream of the powerhouse for up to 8 days, showing a characteristic circling behaviour. Circling eels repeatedly approached the trashrack, sprinted upstream, and finally passed through the turbines with the next high water discharge. These observations are discussed with regard to the design of appropriate downstream passage facilities.     

Exotic silver eels Anguilla anguilla in Japanese waters: seaward migration and environmental factors

To understand the ecology of the exotic silver European eel Anguilla anguilla introduced into Japanese waters, the migratory behavior of 106 specimens captured in the coastal waters of Japan between April 1997 and March 2002 was analyzed. Their migratory behavior was apparently correlated with various environmental factors, particularly photoperiod, water temperature, lunar phase, and passage of atmospheric depressions, and was similar to the behavior of the species in European waters. These findings suggest that transplanted European eels retain their ability to respond to environmental cues for seaward migration in similar temperate habitats. The timing of the migration of silver European eels coincided with that of the native Japanese eels A. japonica, suggesting that the silver European eel was synchronized physiologically with the native eel by the same environmental factors.     

Migration pattern of silver eel (Anguilla anguilla, L.) in an obstructed river system

Abstract –  The downstream migration of European silver eels in the River Frémur was examined to determine the potential effects of the numerous migration barriers that exist on waterways in western France. The Frémur has a 14 m high dam which creates a 3 × 10⁶ m³ water supply reservoir, 6 km from tidal limit. Based on 8-year records (1996–2004) of migrant silver eels captured in a Wolf trap located about 1 km below the dam, the influence of this dam on the migration was examined. These records indicate that 91% of silver eels were captured when the dam was overtopped (i.e. when the water reservoir was full). The timings of the overflow periods varied greatly between years mainly because they are function of the duration of the filling period which in turn is dependent on the level of summer water abstraction and annual hydrological conditions. Consequently, migration periods occurred at variable dates (between November and April) which is late in comparison with nonobstructed European river systems (generally between August and December). During overflow periods the migration of silver eels increased markedly during rain events (increasing river flow). This indicates that flow flushes, are essential so that settled silver eels can orientate themselves and pass over the dam. The hypothesis of a 'dam effect' that could stop temporarily or permanently some of silver eels in the reservoir is discussed. Finally, the influence of the migration delays on the condition of silver eels is considered.     

Decreasing eel stocks: survival of the fattest?

Abstract –  Since the 1980s, the European eel Anguilla anguilla stock is in steep decline. Lipid reserves are essential to cover energetic requirements for silver eel migration and reproduction. Two large and independent data sets from Belgium and The Netherlands show an average one-third decrease in fat contents of yellow eels over the past 15 years. Also Le Cren's relative condition factor decreased. On the basis of the somatic energy reserves, reproductive potential of eels from various latitudes over Europe was estimated, assuming fat levels in yellow eel are indicative of those in silver eels. Only large individuals, females as well as males, with high lipid content seem to be able to contribute to the spawning stock. The decrease in fat content in yellow eels may be a key element in the stock decline and raises serious concerns about the chances of the stock to recover.     

Escapement success and patterns of downstream migration of female silver eel Anguilla anguilla in the River Meuse

Abstract – Downstream migration of female silver eel Anguilla anguilla (L.) was studied by remote telemetry in the lower part of the River Meuse (Belgium and the Netherlands) using a combination of nine detection stations and manual tracking. N = 31 eels (L_T 64–90 cm) were implanted with active transponders and released in 2007 into the River Berwijn, a small Belgian tributary of the River Meuse, 326 km from the North Sea. From August 2007 till April 2008, 13 eels (42%) started their downstream migration and were detected at two or more stations. Mean migration speed was 0.62 m·s^?1 (or 53 km·day^?1). Only two eels (15%) arrived at the North Sea, the others being held up or killed at hydroelectric power stations, caught by fishermen or by predators or stopped their migration and settled in the river delta. A majority (58%) of the eels classified as potential migrants did not start their migration and settled in the River Berwijn or upper Meuse as verified by additional manual tracking.     

Migration of silver eel,Anguilla anguilla,through three water pumping stations in The Netherlands

European eel, Anguilla anguilla (L.), migrating to sea encounter many man-made structures that can hamper and delay migration or induce mortality. Three pumping stations in Friesland, the Netherlands, were covered with acoustic receivers. Ninety-three silver eels tagged with acoustic transmitters were released in the polders upstream of the stations and 89% were detected passing a pumping station. The majority of silver eels passed the stations within a day after arriving at the station. Four silver eels stayed for longer than 2 weeks before passage, and 18 were detected at the receiver downstream the pumping station for more than one day, with detections up to several weeks. These detections probably indicated a dead eel, but could also indicate a live eel remaining at the site. Most of the silver eels passed the pumping stations within a day after release, so fish-friendly pumps will benefit the migrating population most. In the Netherlands, there are several thousand pumping stations. Installing fish passages near these stations is not feasible due to high costs. Prioritising all these sites in relation to the degree of blockage, mortality rates and its relative importance for migratory fish, can maximise the effectiveness of measures and mitigation taken.     

Selective opening of hydroelectric dam spillway gates for downstream migrant eels in New Zealand

Abstract  Selective opening of the Patea hydroelectric dam spillway gates was examined for its potential to provide safe downstream passage for sexually mature (silver) eels in New Zealand. During autumn 2000, one of the spillway gates at the 82-m high Patea Dam was opened for 2.5 h and a large fyke net set across the river about 1.5 km below the dam. Fifty one live endemic longfin eels Anguilla dieffenbachii (Gray), 60 live shortfin eels Anguilla australis (Richardson), and eight dead shortfin eels were captured. All but three of the eels caught were downstream migrants, and aside from the dead eel, only a small portion (5%) had external signs of injury. It was likely that the majority of the eels captured passed over the spillway, but some may have originated from the section of river between the dam and the net or gone through the turbines. To further test the ability of eels to survive passage over the spillway, three controlled spills were made in autumn 2001 and 102 eels released immediately upstream of the partially opened spillway gates. A net stretched across the base of the concrete spillway was used to recover the eels. Most of the eels recovered from the spillway had low levels of injury. However, during the third controlled spill, 10 wild migrant eels were also caught with none showing any external signs of injury. This indicated that the damage noted on the recovered eels were the result of handling rather than passage over the spillway. It was concluded that selective opening of hydroelectric dam spillway gates can provide safe downstream passage for migrant eels.     

Predicting downstream migration of silver eels in a large river catchment based on commercial fishery data

Abstract  Worldwide, populations of catadromous eels are in decline. Knowledge on downstream migration patterns is needed to mitigate damage caused by hydroelectric stations. Silver eel migration and its relation with environmental factors were investigated using data from a fishery located in the lower reaches of a large catchment (110 000 m²). Migration days, indicative of different proportions (50%, 75% and 95%) of the annual run of eels (i.e. represented by the annual catch), were predicted using discriminant analyses. Efficiency of prediction was 58–95% depending on the proportion of the run targeted. The onset of migration was correlated with sunshine hours, August temperature and discharge. Julian days (i.e. photoperiod) was significantly correlated with migration days, indicating between-year similarity in the dynamics of the runs. The size of migrants varied within the migration season, reflecting differences in their initial spatial distribution.     

Effects of silvering state on induced maturation and spawning in wild female Japanese eel <Emphasis Type="Italic">Anguilla japonica</Emphasis>

ABSTRACT:   The effects of silvering state of wild female Japanese eels Anguilla japonica on the success of induced maturation and the following spawning were examined. Thirty-eight females, collected in Mikawa Bay, were divided into four stages based on their silvering state: yellow (Y1), late-yellow (Y2), silver (S1) and late silver eels (S2). Despite injections of salmon pituitary extract (SPE) through the standard technique, Y1 and Y2 eels did not respond to the treatment with undeveloped gonad (gonad-somatic index [GSI]: 0.3–0.9), and all these females died by 5 weeks, probably due to an abnormal physiological condition. Most S1 (81%) and S2 eels (100%) matured completely (GSI: 17.8–51.4), and finally spawned successfully (69% for S1, 89% for S2). S2 eels fully matured with oocytes of over 750 μm in diameter by significantly smaller number of injections of SPE (5–6 times) than the case of S1 eels (6–8 times). The amount of eggs released by S2 eels (0.65 ± 0.11 g/fish per body weight [BW]) was significantly larger than those by S1 eels (0.54 ± 0.09 g/fish per BW). There was no difference in fertilization and hatching rates between eggs released by S1 eels and those of S2 eels. These results indicate that the success of induced maturation and spawning in wild female Japanese eels depends on their silvering state, and matured eggs can be obtained efficiently through the use of S2 eels rather than other stages.     

Gonad histology and plasma steroid profiles in wild New Zealand freshwater eels (Anguilla dieffenbachii and A. australis) before and at the onset of the natural spawning migration. I. Females*

To determine steroid profiles in immature and maturing female eels from the wild, non-migratory and migratory New Zealand longfinned (Anguilla dieffenbachii) and shortfinned (A. australis) eels were caught and blood and ovarian samples collected. Plasma steroid levels were determined and related to the developmental stage of the ovary. Ovaries of non-migrants contained oogonia and previtellogenic oocytes. Vitellogenic oocytes were never observed in these groups, but instead were very common among migrants (up to 88% of oocytes). Concentrations of both androgens (androstenedione (AD), testosterone (T)) and estradiol-17 (E2) were higher in migrants than in non-migrants. Among migrants, T levels were higher in shortfins (2.27 ± 0.14 ng ml–1) than in longfins (0.82 ± 0.10 ng ml–1), whereas E2 levels were higher in longfins (mean 2.46 ng ml–1) than in shortfins. Levels of sex steroids were generally low in non-migrants. In contrast, plasma levels of 17-hydroxyprogesterone were significantly higher in non-migrants than in migrants. Similarly, cortisol levels were higher in non-migrating than in migrating shortfinned, but not longfinned, females. 17,20-Dihydroxy-4-pregnen-3-one, the putative maturation-inducing steroid in anguillids, was near minimum-detectable levels for all animals examined. Surprisingly, very high levels of 11-ketotestosterone (KT) were found in migrants, averaging nearly 3 ng ml–1 in longfins and over 20 ng ml–1 in shortfins. The identity of KT and several 5-reduced androgens was confirmed using gas chromatography - mass spectrometry. The function of KT in females is not known, but we suggest that this steroid hormone may play a role in preparing maturing animals for their spawning migration.     

Lipid content and fatty acid composition of muscle,liver, ovary and eggs of captive-reared and wild silver Japanese eel <Emphasis Type="Italic">Anguilla japonica</Emphasis> during artificial maturation

ABSTRACT:   Changes in lipid content and fatty acid composition of muscle, liver and ovary of captive-reared and wild silver Japanese eel Anguilla japonica were examined during artificial maturation induced by salmon pituitary homogenate (SPH) injections. Although the relative levels of n-3 and n-6 highly unsaturated fatty acids (HUFA) in liver and ovary were higher than in muscle in both captive and wild silver eels before SPH injection, these tended to decrease with maturation. The relative levels of n-6 HUFA in muscle, liver, ovary and eggs of wild silver eels were remarkably higher than those in captive eels. Therefore, we attempted to alter the ratio of n-6 HUFA in eggs by feeding eels a diet supplemented with linoleic acid-rich plant oil. Although the percentage of n-6 polyunsaturated fatty acids to total fatty acids in eggs of eels fed the supplemented diet was similar to wild silver eels, the percentage of n-6 HUFA remained remarkably lower than in wild silver eels. Hence, it appears that the supplemented diet affected the fatty acid composition of eggs, but did not result in much conversion of linoleic acid to its higher homologs in eels.     

Controlled reproduction in Anguilla anguilla (L.): comparison between spontaneous spawning and stripping‐insemination approaches

This study aimed to compare the fertility of eggs between artificially matured female silver eels that spawned spontaneously and those that were spawned by manual stripping. The effects of the two methods of spawning on ovulation and fertilization rate were also investigated. For this purpose, 18 wild female European eels captured in Bonello lagoon (North Adriatic Sea) were carp pituitary extract‐injected to undergo sexual maturation and ovulation; a final injection of 17,20β‐dihydroxy‐4‐pregnen‐3‐one (DHP) was administered when at least 30% of the oocytes were fully transparent. After the DHP‐injection, nine eels were transferred to a new closed recirculating aquaculture system, where they were housed with spermiating males (sex ratio 4/1) to allow spontaneous spawning (SPT‐group); the remaining nine eels were transferred to a 250 L tank and ovulation was checked at four‐hourly intervals by manual stripping (STR‐group). The number of eggs per female in the SPT‐group was significantly greater than that in the STR‐group. Furthermore, fertilization rates in the SPT‐group were notably higher than those observed in the STR‐group. Significantly, the best performances were obtained among eels in which at least 50% of oocytes were fully transparent at the time DHP was administered. We conclude that the fertility of eggs from spontaneously spawning eels is superior to that of eggs acquired by strip‐spawning and artificial fertilization.     

Patterns of oocyte development in natural habitat and captive <Emphasis Type="Italic">Salminus hilarii</Emphasis> Valenciennes, 1850 (Teleostei: Characidae)

Fecundity and oocyte development in Salminus hilarii female brood stock were analyzed with the aim of investigating the impact of migration impediment on oogenesis. Histological analyses of the ovaries were performed in adult females caught in two different environments—the Tietê River (natural) and captivity—and the gonadossomatic index, oocyte diameter and fecundity determined. Five germ cell development stages (oogonium, perinucleolar, cortical alveoli, vitellogenic, ripe) and two other structures (postovulatory follicles and atretic oocytes) were observed in females caught in the river. Captive animals lacked the ripe oocytes and postovulatory follicles and had a relatively higher number of atretic oocytes. Females in captivity are known to produce larger oocytes, and they release fewer eggs in each spawn (absolute fecundity) when compared with animals that are able to migrate. Our results suggest that the Tietê River is undergoing alterations which are being reflected in the reproductive performance of S. hilarii, mainly due to the presence of atretic oocytes in females caught in the river. The lack of postovulatory follicles and ripe oocytes in captive animals reveals that migratory impediment negatively impacts final oocyte maturation. However, the stage of maturation reached is adequate for ovulation induction with hormone manipulation.     

Modification of essential fatty acid composition in broodstock of cultured European eel Anguilla anguilla L

Farmed eels had lower levels of arachidonic acid (20:4 n‐6) (ARA) and higher ratios of eicosapentaenoic acid (20:5 n‐3) (EPA):ARA compared to wild European eels collected from the Baltic Sea and southern Norwegian coast. Eels fed a formulated feed (JD) with a distribution of essential fatty acids (EFA) resembling wild European eel were sampled after 0, 5, 10, 14 and 44 weeks of feeding to examine changes in fatty acid composition (FAC) in ovaries, visceral fat and muscle. The results showed a slow but steady incorporation of EFA. Lipids are incorporated in the oocytes early in oogenesis, and the leading cohort of oocytes is rich in lipid droplets before the onset of vitellogenesis. This indicates that feeding with optimized broodstock feeds should start early to allow the incorporation of EFA in the first cohort of oocytes. At least 14 weeks of feeding is required to change lipid EFA in broodstock eel to resemble EFA in the diet or in wild fish. After 44 weeks of feeding, ARA was significantly higher in the neutral lipids of ovaries (1.9%) compared to visceral fat (1.2%) or muscle (1.0%). EPA:ARA ratios decreased two‐ to threefold in all tissues examined during that time. ARA and docosahexaenoic acid (22:6 n‐3) (DHA) had accumulated in ovarian polar lipids.     

Positive feedback control by the gonads on gonadotropin (GTH) and gonadoliberin (GnRH) levels in experimentally matured female silver eels,Anguilla anguilla

Treatment of sham-operated female silver eels with carp pituitary extract stimulated ovarian development and induced increases in pituitary gonadotropin (GTH) and gonadoliberin (GnRH) contents. Both effects of carp pituitary extract were abolished in ovariectomized eels, indicating the involvement of the gonads. Endogenous sexual steroids, the secretion of which was increased during sexual maturation, should be responsible for the stimulation of GTH and GnRH levels. Ovariectomy itself had no significant effect on pituitary GTH and GnRH contents, reflecting the fact that, at the silver stage, sexual steroid levels are too low to exert any significant effect on pituitary GTH and GnRH. The positive feedback control exerted by the gonads on GTH and GnRH levels during sexual maturation, in the eel as well as in some other teleosts, would produce an amplification of the pubertal stimulation of the hypothalamo-pituitary-gonadal axis.