Ecological Aspects of the Downstream Migration of Introduced European Eels in the Uono River, Japan

We examined the species composition, timing of downstream migration, and biological characteristics of eels using catches at three commercial weirs from 1996 to 1998 in the Uono River, Niigata Prefecture, Japan, which is located farther north in the Japan Sea than where most Japanese eels, Anguilla japonica, recruit. Analyses of a sub-sample of the 292 eels caught in the weirs found that 93.6% were introduced European eels, Anguilla anguilla, that were sexually maturing silver phase eels. Their average age based on otolith annuli was 10.2 years, indicating a relatively high average growth rate of 6.3 cm year^–1. Catch records in 1996 and 1997 indicated that downstream migration occurred sporadically from the middle of August to the end of November and that catches generally coincided with abrupt increases in water discharge and drops in water temperature. The highest catches in both years occurred between the last quarter and new moon. These findings were similar to studies on this species in Europe and indicate that A. anguilla can grow rapidly, begin maturation, and start downstream migration far from its native range. This discovery of introduced eels initiating their spawning migration at the same time as A. japonica raises concerns about the potential impact of interbreeding between species and the possible effects on the fishery resources of A. japonica.     

Ovarian morphology of the Japanese eel in Mikawa Bay

Annual changes in gonadal maturation of female Japanese eel Anguilla japonica in sea water were investigated histologically over 5 years in the Mikawa Bay, Japan, where they occurred throughout the year except in March. Almost all immature Japanese eels (yellow eels) occurred mainly from April to September, and they were rare after November. In contrast, maturing Japanese eels (silver eels) occurred from October to February. The gonado‐somatic index ( I _G) and oocyte diameters of yellow eels were <1·0 and 150 μm, respectively, and oocytes were at the peri‐nucleolus or the oil droplet stages. The I _G and oocyte diameters of silver eels were greater than those of yellow eels and most oocytes developed to the primary yolk globule stage. The numbers of silver eels lacking oocytes at the primary yolk globule stage increased after January in Mikawa Bay, although I _G and oocyte diameters remained unchanged. In contrast, silver eels caught at the mouth of the bay in January possessed oocytes that had advanced to the secondary yolk globule stage. These observations indicate that oocyte development changes seasonally, especially after winter in Mikawa Bay.     

Sex Determination in Freshwater Eels and Management Options for Manipulation of Sex

Catadromous eels enter fresh water as sexually undifferentiated glass eels and develop into males and females before migrating back to sea as silver eels. Females develop ovaries directly from the ambiguous primordial gonad whereas males pass through a transitional intersexual stage before developing testes. Eels have sex-specific life-history strategies. Males may grow faster than females initially, but this difference is soon reversed and females attain a greater age- and size-at-metamorphosis than males. Male fitness is maximized by maturing at the smallest size that allows a successful spawning migration (a time-minimizing strategy) whereas females adopt a more flexible size-maximizing strategy that trades off pre-reproductive mortality against fecundity. Although heteromorphic sex chromosomes have been identified in some species, the sex of developing gonads is labile and gender is determined principally by environmental factors. Individuals experiencing rapid growth prior to gonad differentiation tend to develop as males, whereas eels that grow slowly initially are more likely to develop as females. Paradoxically, males tend to predominate under conditions of high density, which may be because a male “grow quickly, mature early” strategy increases an individual’s chances of survival during periods of intraspecific competition. High temperatures and saline conditions have also been proposed to favor development as males but experimental studies have failed to demonstrate a clear effect of either on sex determination. High proportions of female silver eels migrating from some upstream areas, lakes and large rivers may be due to low population density or poor conditions for growth in these habitats. Manipulating sex ratios in favor of females has the potential to increase eel production in aquaculture and to buffer natural populations against fishing pressure. Sex steroids (oestrogens and phytoestrogens) have a strong feminizing effect on undifferentiated individuals and are most effective when targeted at younger eels and administered at high doses for prolonged periods. Modifying local environmental conditions, in particular reducing eel density and limiting interference and social stress, may also promote the development of females. Further research into the timing and mechanisms of sex determination in eels is required to effectively and efficiently manipulate sex for conservation and/or economic benefit.     

Glycolytic fluxes in European silver eel, Anguilla anguilla: sex differences and temperature sensitivity

European silver eels migrate 6000 km to their supposed spawning area in the Sargasso sea. As the eel is fasting, this intense swimming activity is realised only with fat stores, involving mainly red muscle i.e. aerobic metabolism. However, eel migration is performed at depth and thus in cold water, both being known to induce changes in muscle energy metabolism. During migration, white and red muscles can operate together or separately in order to counteract the eventual effects of low temperatures and/or high pressures. We have studied the temperature sensitivity (5, 15, and 25 °C) of aerobic and anaerobic metabolism in both sexes. At the same temperature, migrating eels have a higher basal glycolytic flux. Moreover, there are temperature and sex effects: anaerobic glycolysis (JB) is more sensitive to cold water whereas aerobic (JA) is more affected by warm. Males, which are less sensitive to cold water, also have higher aerobic fluxes than females. As depth corresponds to low temperature, the possibility that males migrate more deeply than females is discussed. In an ecophysiological context, it is interesting to suppose that males and female eels migrate at different depths in order to optimize their energy utilization by aerobic and / or anaerobic pathways.     

Experimental test of environmental factors influencing the seaward migration of European silver eels

In this study we test which environmental factors are influencing the migratory behaviour of seaward migrating silver European eets Anguilla anguilla in a Norwegian river. We test this by transplanting tagged silver eels upriver after catching them in a trap at the outlet of the river. We did this at four fixed dates (fixed day lengths) during 5 years. Over 74% of the variation in time from release to subsequent recapture could be accounted for by variation in time at release, water discharge at release, and moon phase at release (in decreasing order of importance). The number of days to median day of recapture of each batch decreased as the season progressed and decreased with increasing water discharge. Water temperature did not explain any of the remaining variation in the model, even if there was a significant correlation between water temperature at release and median day at recapture of each batch (in simple linear regression model). Recapture rate during the same migration season varied strongly with water temperature, but at most 33% of the variation could be explained by this factor. It was aiso evident that the recapture rate increased when the number of downward migrating untagged silver eels was high. Day length (i.e. time at release) did not explain any of the remaining variation in recapture rate.     

Olfactory clues play a critical role in the estuarine migration of silver-phase American eels

Estuarine migration of anosmic and control silver-phase American eels was examined during the fall spawning migration. Ultrasonic telemetry was used to track seventeen control and eight anosmic silver eels through 32 km of the Penobscot Estuary, Maine, U.S.A.. Twelve of seventeen control eels migrated out of the estuary in 97 h (approximately 4 d) on average. Only two of eight anosmic eels migrated out of the estuary. On average these two anosmic eels migrated out of the estuary within 180 h (approximately 7.5 d) of release and the other six had not left within 9 d. Most control eels progressed rapidly to the mouth of the estuary within a few days. Anosmic eels spent more time in the estuary and demonstrated different behavior from control eels due to their lack of olfaction. Some control eels moved with the appropriate tide, the ebb tide for transport out of the estuary, within one tidal cycle of being released into tidal freshwater. However, anosmic eels either did not move with the appropriate tide or took significantly longer to do so. Olfaction was probably used for orientation by control eels sensing chemical clues (organic and inorganic), which change throughout the tidal cycle. Increased migration times and errors in orientation were likely related to the inability of anosmic eels to use selective tidal stream transport for movement out of the estuary. Chemical clues seem to be one of the most important environmental clues used to guide estuarine migration of silver eels. However, a hierarchy of sensory mechanisms and environmental clues are most likely used for estuarine orientation.     

Differences in size and growth rates of male and female migrating Japanese eels in Pearl River, China

The Sr/Ca ratios in otoliths of silver Japanese eels Anguilla japonica , in Pearl River, China, indicated that both sexes did not stay in brackish water and grew in fresh water from the glass eel stage until spawning migration. This did not support the hypothesis that females tended to distribute upstream and males might be restricted to estuaries. The back-calculated total length of males at glass eel stage was not significantly different from that of females, indicating that the hypothesis that small glass eels became males and larger ones became females may not be true. The mean (±S.D.) age and total length of males at migration were 6·4±1·6 years and 48·3±4·5 cm, which were significantly smaller than for females, 8·3±1·6 years and 61·4±4·1 cm. The age of migration was related inversely to growth rate for both sexes. Growth parameters of the von Bertalanffy growth equation were K =0·21 cm year°1, L _∞=55·7 cm and t _o=-0·55 year for males and K =0·14 cm year⁻¹, L _∞=77·5 cm and t _o=-0·60 year for females. The difference in asymptotic length ( L _∞) between males and females may be because females postpone migration to achieve larger size for maximizing reproductive success.     

Thermal preferenda and behavior of Atlantic eels (genus Anguilla) in relation to their spawning migration

Synopsis The final preferred temperatures (FPTs) of adult premigratory and migratory life-history phases of American eels, Anguilla rostrata, were determined by chronic tests in a horizontal thermal gradient. Mean FPTs were between 17 and 20°C and were not significantly different between life-history phases, acclimation temperatures, illumination regimes, photoperiods or sexual maturation states. Thermal behavior of eels was highly variable, both among individuals of the various test groups and among repeated tests of single individuals. Light inhibited behavioral thermoregulation by promoting shelter-seeking. The following inferences are drawn from the laboratory findings and observations of migrating A. rostrata and A. anguilla (European eels) in the North Atlantic: (1) decreasing temperatures may initiate downstream migration of silver eels, (2) eels may select temperatures close to their FPT in thermally stratified environments, but will tolerate higher and lower temperatures depending on illumination or other physical constraints, (3) the oceanic phase of the migration to the Sargasso Sea may take place at relatively shallow depths in the open ocean, probably within the upper 1000 meters. The strong eurythermality observed in eels may facilitate their occupation of and migration through thermally diverse and unpredictable habitats.     

Shark Predation on Migrating Adult American Eels (Anguilla rostrata) in the Gulf of St. Lawrence

In an attempt to document the migratory pathways and the environmental conditions encountered by American eels during their oceanic migration to the Sargasso Sea, we tagged eight silver eels with miniature satellite pop-up tags during their migration from the St. Lawrence River in Québec, Canada. Surprisingly, of the seven tags that successfully transmitted archived data, six were ingested by warm-gutted predators, as observed by a sudden increase in water temperature. Gut temperatures were in the range of 20 to 25°C—too cold for marine mammals but within the range of endothermic fish. In order to identify the eel predators, we compared their vertical migratory behavior with those of satellite-tagged porbeagle shark and bluefin tuna, the only endothermic fishes occurring non-marginally in the Gulf of St. Lawrence. We accurately distinguished between tuna and shark by using the behavioral criteria generated by comparing the diving behavior of these two species with those of our unknown predators. Depth profile characteristics of most eel predators more closely resembled those of sharks than those of tuna. During the first days following tagging, all eels remained in surface waters and did not exhibit diel vertical migrations. Three eels were eaten at this time. Two eels exhibited inverse diel vertical migrations (at surface during the day) during several days prior to predation. Four eels were eaten during daytime, whereas the two night-predation events occurred at full moon. Although tagging itself may contribute to increasing the eel''s susceptibility to predation, we discuss evidence suggesting that predation of silver-stage American eels by porbeagle sharks may represent a significant source of mortality inside the Gulf of St. Lawrence and raises the possibility that eels may represent a reliable, predictable food resource for porbeagle sharks.     

Low fat contents in female silver eels: indications of insufficient energetic stores for migration and gonadal development

The main energetic stores at the silver eel stage were studied by analysing muscle fat concentrations and hepatosomatic indices in female silver eels from various habitats in Sweden. Muscle fat concentrations varied both within and between localities and lean eels with muscle fat concentrations <20% occurred at all study sites. Furthermore, no correlation could be found between muscle fat content and internal or external maturation indices, neither was the relative liver size related to the maturation process, as the correlation between the hepatosomatic and gonadosomatic indices was very weak. Consequently, it was concluded that silvering and the spawning migration may begin also at low muscle fat concentrations. However, most of the energy reserve is stored as muscle fat in eel, and it is highly unlikely that female silver eels with such low fat contents, as were observed occasionally in this study, will ever recruit to the next generation. Therefore, it is suggested that the maturation process in eel is more flexible than previously recognized, and that this process might be temporarily arrested and feeding resumed during the first part of the migratory phase.     

A biological analysis of eel catches, Anguilla anguilla L., from the lagoons of Lesina and Varano, Italy

A study of eel catches from Lesina (444 specimens) and Varano lagoons (325 specimens), in southern Adriatic, Italy, was made. Male silver eels in Lesina ranged from 33.4–51.5 cm in length, with a mean of 42.6 cm; from 50–240 g in weight, with a mean of 141 g and were 1.5–6.5 years old with a mean of 2.5 years. The average length of male silver eels in Varano lagoon was 40.5 cm (range 31–48.5 cm); the average weight was 122 g (range 80–220 g)and a mean age of 2.6 years (range 1.5–7.5 years).
The females are bigger, heavier and older than the males with, in Lesina, a mean length of 61 cm (range 50.9–74.3 cm), a mean weight of 438 g (range 240–730 g) and a mean age of 3.4 years (range 1.5–6.5). The average length of Varano female silver eels was 58 cm (range 50.8–72.5 cm), and the average weight was 383 g (range 225–840 g). They were 1.5–7.5 years old, with an average of 3.8 years. Female silver eels were only 20% of the population at Lesina and 10% at Varano.
In comparison with the silver eel populations of the North Adriatic lagoons, the North Sea or the Atlantic Ocean, the silver eels of Lesina and Varano show a greater growth rate, are younger and have a sex ratio in favour of the males.
The water temperature, higher than in other countries, could be an important factor affecting the differences in age and growth rates between Lesina and Varano silver eels and those of other waters.     

Growth rate and age at migration of Anguilla anguilla

The length, age and growth rate were investigated for downstream migrating male and female eels in the unexploited Burrishoole system, western Ireland. Significant differences were found in the age and length at migration with the larger, older female eels also showing faster annual growth as early as the first year in fresh water. Female eels normally migrated at lengths from 40.5 cm, exceptionally to 92.9 cm, and male eels at lengths between 28.9 and 46'0 cm. Back-calculation showed an irregular pattern of fast and slow annual growth. Mean annual growth increments were almost always greater for females than for males.     

Timing and pattern of annual silver eel migration in two European watersheds are determined by similar cues

Many animals perform long‐distance migrations in order to maximize lifetime reproductive success. The European eel migrates several thousand kilometers between their feeding habitats in continental waters (fresh‐, brackish, and sea water) and their spawning area in the Sargasso Sea. Eels residing in freshwaters usually initiate their spawning migration as silver eels during autumn, triggered by diverse environmental cues. We analyzed the time series of silver eel downstream migration in Burrishoole, Ireland (1971–2015), and Imsa, Norway (1975–2015), to examine factors regulating the silver eel migration from freshwater to the sea. The migration season (90% of the run) generally lasted from 1 August to 30 November. Environmental factors acting in the months before migration impacted timing and duration of migration, likely through influencing the internal processes preparing the fish for migration. Once the migration had started, environmental factors impacted the day‐to‐day variation in number of migrants, apparently stimulating migration among those eels ready for migration. Both the day‐to‐day variation in the number of migrants and the onset of migration were described by nearly identical models in the two rivers. Variables explaining day‐to‐day variation were all associated with conditions that may minimize predation risk; number of migrants was reduced under a strong moon and short nights and increased during high and increasing water levels. Presence of other migrants stimulated migration, which further indicates that silver eel migration has evolved to minimize predation risk. The onset of migration was explained mainly by water levels in August. The models for duration of the migration season were less similar between the sites. Thus, the overall migration season seems governed by the need to reach the spawning areas in a synchronized manner, while during the actual seaward migration, antipredator behavior seems of overriding importance.     

Light-Sensitive Vertical Migration of the Japanese Eel Anguilla japonica Revealed by Real-Time Tracking and Its Utilization for Geolocation

Short-time tracking (one to eight days) of the Japanese eel (Anguilla japonica) using ultrasonic transmitter was performed in the tropical-subtropical area adjacent to the spawning area and temperate area off the Japanese Archipelago. Of 16 eels (11 wild and five farmed) used, 10 wild eels displayed clear diel vertical migration (DVM) from the beginning, while the other five farmed eels tracked for 19 to 66 hours did not. During daytime, a significantly positive correlation between migration depth and light intensity recorded on the vessel was observed in the 10 wild eels, indicating that the eels were sensitive to sunlight even at the middle to lower mesopelagic zone (500 to 800 m). During nighttime, the eel migration depth was observed to be associated with the phase, rising and setting of the moon, indicating that the eels were sensitive to moonlight at the upper mesopelagic zone (<300 m). Two of 10 wild eels were in the yellow stage but shared similar DVM with the silver stage eels. Swimbladders of three silver stage eels were punctured before releasing, but very little effect on DVM was observed. The eels very punctually initiated descent upon nautical dawn and ascent upon sunset, enabling us to determine local times for sunrise and sunset, and hence this behavior may be used for geolocating eels. In fact, estimated positions of eels based on the depth trajectory data were comparable or even better than those obtained by light-based archival tag in other fish species.     

A comprehensive hypothesis on the migration of European glass eels (Anguilla anguilla)

The European eel (Anguilla anguilla) is a catadromous fish that spawns in the Sargasso Sea. As larvae, eels cross the Atlantic Ocean and reach the continental slope of Europe, where they metamorphose into post‐larval glass eels. These reach the continent, where some enter fresh water, some remain in marine waters, and others move between fresh and marine waters. After 5–25 years, as adult silver eels, they migrate back from fresh water to the Sargasso Sea to spawn and die. The glass eel stage is a critical step during which the eels cross the continental shelf and recruit to estuaries, where they facultatively transition to fresh water. Extensive research has been conducted to understand the behavioural mechanisms and environmental cues that aid and guide glass eels' migration. Glass eels follow odours and salinity gradients, they avoid light, and they change orientation and depth according to the tides. Recent work revealed that European glass eels also use Earth's magnetic field and lunar cues to orient. However, while we understand many aspects of their orientation behaviour, a unifying theory describing how glass eels migrate from the continental slope to fresh water is lacking. The goal of this review is to develop a comprehensive hypothesis on the migration of European glass eels, integrating previous knowledge on their orientation behaviour with recent findings on magnetic and celestial orientation. This review follows the journey of a hypothetical glass eel, describing the nature and the role of orientation cues involved at each step. I propose that, although glass eels have the sensory capacity to use multiple cues at any given time, their migration is based on a hierarchical succession of orientation mechanisms dictated by the physical properties of the environments that they occupy: (i) lunar and magnetic cues in pelagic water; (ii) chemical and magnetic cues in coastal areas; and (iii) odours, salinity, water current and magnetic cues in estuaries.     

Three-dimensional migratory behaviour of European silver eels (Anguilla anguilla) approaching a hydropower plant

The global population of European eel (Anguilla anguilla) is rapidly declining, and migration barriers in rivers are believed to be one of several key causes. While progress has been made in the development of bypass solutions, they are often constructed based on a limited knowledge of swimming behaviour. A bypass close to the stream bed is often recommended at fish passage facilities to accommodate downstream eel migration. The results of this recommendation are poorly studied, and the few studies that exist show varying bypass efficiencies. The current study used acoustic telemetry with depth sensors to explore the three-dimensional migratory behaviour of downstream-migrating silver eels. The eels were tracked as they approached a hydropower plant with a state-of-the-art angled bar rack and full-depth bypass. Downstream and upstream swimming differed in preferred vertical and lateral positions. During periods of local downstream movement, the density of observations was largest in the upper middle section, away from the river boundaries and in higher velocities. Conversely, when moving upstream, eels tended to avoid the upper layers of the middle part of the river, swimming closer to the riverbed and using the bank areas to a greater extent. Downstream-moving fish swam higher in the water column during night and in turbid conditions (high discharge). When approaching the impassable bar rack and the full-depth bypass, the eels searched most intensely but not exclusively along the bottom third of the rack, often exploring at new depths after changing direction. The impediment passage efficiency was 100% when both bypass solutions were considered. The study provides knowledge of the swimming behaviour of silver eels, which is relevant for the design of bypass solutions for eels at migration barriers.     

Are Lithuanian eels fat enough to reach the spawning grounds?

Stocks of the European eel Anguilla anguilla have been in a steep decline since the 1980s. Stocking of water bodies with juvenile eels captured in the wild to establish or enhance local populations has been a common practise in Europe for many decades. However, the degree of contribution by stocked eels to natural spawning capacity is poorly known and extensively debated. There have been suggestions that eels derived from stocking are less likely to contribute to the spawning stock due to a lack of navigational capability and lower fitness related to insufficiency of energetic resources. Results of the current study indicated that eels translocated long distances from the point of capture and released into inland waters in Lithuania are successfully undergoing the silvering process. A proportion of 23.7% (N = 27) among all migrating eels were described to be at the yellow (SI, SFII or SFIII) eel stage and downstream movements of these eels should be attributed to local movements, rather than spawning migration; 76.3% were assigned to the silver eel stage. This study suggests that 36.8% (N = 32) of downstream migrating silver eels of stocked origin had accumulated sufficient energetic resources for spawning migration and gonadal development and should be able to traverse the 7900-km distance to the presumptive spawning grounds in the Sargasso Sea. The rest of migrating silver eels (63.2%, N = 55) had insufficient energetic resources; the average potential swimming range of these eels was estimated to be 6135 ± 683 km.     

Evidence for Environmental Sex Determination in the American eel, Anguilla rostrata

Males have predominated among migrating silver eels in the Annaquatucket River, Rhode Island, for at least two decades, with no significant variation in mean total length in either sex. Because the species is panmictic (random breeding), this consistency suggests environmental sex determination (ESD). Most yellow (feeding phase) eels <300mm total length in the Annaquatucket are sexually undifferentiated, and in contrast to all other published sex ratios, males greatly outnumber females (3:1) among differentiated yellow eels. Estimates of yellow eel population densities are 4–10 times greater than published values for other habitats. We propose that this crowding results in a long period of undifferentiation and the suppression of femaleness. Published field and experimental evidence indicates that high population density results in high proportions of males in Atlantic Anguilla, and that low population density results in the predominance of females. This ESD may be adaptive, resulting in vast numbers of small males in coastal habitats, relatively close to the spawing area, and much larger and more fecund females that occupy most of the available eel habitat.     

Advanced sexual maturation before marine migration of Anguilla bicolor bicolor and Anguilla marmorata at Réunion Island

Maturing sub-adults of two species of anguillid eels (a female Anguilla bicolor bicolor and a male Anguilla marmorata ) were collected for the first time at Réunion Island, western Indian Ocean. Both were silver eels, i.e. maturing eels at the onset of their spawning migration, and characterized by advanced sexual maturation that has been only observed in Anguilla dieffenbachii from New Zealand.     

Swimming performance of silver eels is severely impaired by the swim-bladder parasite Anguillicola crassus

Infection with the swim-bladder parasite Anguillicola crassus is suggested as one of the principal causes of the collapse of the European eel population. This nematode has been introduced in Europe from Asia in the 80s and parasitized in a short time Anguilla eel species in different geographical regions across the globe. The parasites drain energy due to their sanguivorous feeding and they cause mechanical damage on the swim-bladder wall. These two effects are hypothesized to impair the spawning migration of the European eel. In this study, we have investigated both effects on swimming performance. We hypothesized that parasitic sanguivorous activities - related to parasite weight - reduce swimming endurance, while mechanical damage of the swim-bladder impairs buoyancy control. Eighty eels suffering various degrees of infection were introduced in swim-tunnels and subjected to a swimming fitness test. The relation between A. crassus infection and swimming efficiency was measured for large female silver eels swimming at various speeds. Infected eels had lower cruising speeds and a higher cost of transport. Eels without parasites, but with a damaged swim-bladder showed similar effects. Almost half of the eels that contained damaged swim-bladders (43%) stopped swimming at low aerobic swimming speeds (< 0.7 m/s). Simulated migration trials in a recent related study have confirmed that eels with a high parasite level or with damaged swim-bladder show early migration failure (< 1000-km). Reduced swimming performance appears to be associated with swim-bladder dysfunction. As we found that especially silver eels have much higher infection levels than yellow eels, it is concluded that migrating silver eels with severely infected or damaged swim-bladders are unable to reach the spawning grounds.