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.     

Environmental factors affecting migration of the European eel in the Rivers Severn and Avon, England

Studies were conducted during 1991–1993 on environmental factors affecting the upstream migration of eels in the Rivers Severn and Avon, England. Migrants (> 156 000 pigmented elvers and > 189 000 juveniles) were trapped as they attempted to ascend weir or sluice barriers. Multiple regression models were developed to compare catches per trap per night (C) with data for various key environmental parameters at seven sites, from the tidal limit to a maximum of 42.5 km upstream. The key stimulus for migration of both elvers and juveniles at the tidal limit was water temperature, with some weaker monthly influences related to seasonal temperature increases. Smaller annual influences probably related to earlier glass eel recruitment into the lower estuary. A weak early tidal effect was demonstrated only once, in 1993 in the Severn. Temperature also exerted significant effects on C of juvenile eels at the tidal limit and in the non-tidal rivers, although effects weakened with distance upstream. Year, month, river flows and whether traps were mounted on weirs or sluices made only small contributions at a few sites. Distance between traps also contributed to combined data for upper Severn sites. The threshold temperature in all cases was 14–16°C, with low to zero catches below 10–11°C, catch maxima being achieved above 18–20°C. The implications of strong temperature-dependence of migration in relation to stock recruitment and management are discussed. Special reference is made to recent decreases in recruitment of eels to Europe and N. America and possible long-term effects of global warming.     

Long-term numerical changes and regulation in a river stock of European eel Anguilla anguilla

1. The objective was to explore the regulatory mechanisms underlying the numerical dynamics of a river stock of European eel Anguilla anguilla based on a purely observational study. We used a 21-year data set on the Rio Esva (Asturias, northwestern Spain) stock of eels, encompassing eel density at an estuary site and at nine sites distributed among three tributaries selected to differ in the distance from the tidal limit and fishery data on glass eels from the nearby Rio Nalón estuary.
2. The abundance of glass eels and estuarine and in-stream densities declined simultaneously over a 15-year period. However, following a historical minimum in the abundance of glass eels around the year 2000, the density continued to decline in the estuary whereas density in the streams began an increase that has continued to the present.
3. In-stream cohort mortality rate ( Z ) varied from 0.0016 day⁻¹ to only 0.0003 day⁻¹ (on an annual basis from 0.57 to 0.099 year⁻¹). The negative effects of intra-cohort and inter-cohort densities on mortality rate emphasized the responses of the riverine stock to compensatory density-dependence. As a consequence, the number of eels surviving to commence the silvering stage was similar in magnitude in the strongest and weakest cohorts.
4. These results suggest that, even if the low abundance of glass eels persists, in-stream density may increase towards a stable value regulated by in-stream density-dependence.     

Intraseasonal characterization of glass eel migration in the River Tiber: space and time dynamics

Glass eel ( Anguilla anguilla ) upstream migration was studied in the River Tiber estuary to obtain a better understanding of spatial and temporal migration dynamics within the season of ascent. Using data from glass eel fisheries, time series analysis of daily catches per unit of effort revealed a fortnightly cycle that can be related to invasion waves possibly corresponding to tidal currents. The amplitude of these waves appeared to correspond to the tidal area of the estuary. Furthermore, glass eels apparently had a delay in this area before resuming upstream migration.     

The role of a freshwater tidal area with controlled reduced tide as feeding habitat for European eel (Anguilla anguilla,L.)

Implementation of the Controlled Reduced Tide (CRT) technique could increase the total surface of tidal freshwater marshes in Europe and ease implementation of restoration projects in coastal defense and riverine ecosystems. The goal was to determine whether a regularly flooded area connected to a freshwater tidal river could act as an important foraging area for European eel, and if so, to what extent the diet of eels in this flooding area differed from that of eels foraging in the river itself. The stomach contents of eels from the River Schelde were compared with eels from the Lippenbroek, an adjacent CRT area. Prey diversity (H′) of individual eels was about four times higher in the Lippenbroek than in the River Schelde. Moreover, 12 prey categories in eel stomachs from the Lippenbroek were found whereas only three categories were retrieved from eels in the River Schelde. In the Lippenbroek, eels fed on terrestrial organisms (lumbricids, caterpillars and other insects), but also on fish and fish eggs and to a lesser extent on other aquatic prey (Lumbricullidae, chironomids and Hirudinea). In contrast, eels from the main river fed mainly on tubificids, fish, and some gammarids. Consequently, eels in the Schelde estuary are opportunistic feeders, but with a preference for large benthic prey. The number and weight of aquatic organisms ingested by eels in the Lippenbroek is not significantly different from the River Schelde. However, eels foraging in the Lippenbroek area had consumed significantly more terrestrial prey. Furthermore the total caloric value estimated for the ingested prey of eels from the Lippenbroek (derived from the literature) was about twice as high as that for eels from the River Schelde. While the condition index remained inconclusive, an Ancova revealed that eels captured in the Lippenbroek were significantly heavier for a given length than eels captured in the Schelde. The study showed that with a controlled reduced tide to restore lateral connectivity of large tidal rivers with their adjacent floodplains, high quality habitats for the European eel are created. These measures could significantly contribute to the production of eels in better condition, which have better chances to reproduce successfully. Hence, wetland restoration could enhance the recovery of the European eel stocks.     

Decline in non-native freshwater eels in Japan: ecology and future perspectives

The occurrence, distribution, and biological characteristics of non-native freshwater eels were analyzed using 5524 eels collected from 16 sites in Japan between 1997 and 2005. Three hundred seventy-four fishes (6.8%) were identified as non-native European eels, Anguilla anguilla, while the remainder (93.2%) were native Japanese eels, A. japonica. The European eel was found at 7 sites (44%), including 3 rivers, 2 freshwater lakes, one brackish lake, and one sea bay, suggesting a wide rage of habitat use. This variability of habitat use was also evidenced by the otolith microchemistry, which showed that they had lived in not only freshwater but also in seawater habitats. The sites with European eel were localized within the vicinity of southern Japan where a number of these eels were cultivated in the early 1970’s, suggesting that some had escaped from the culture ponds or were released intentionally into nearby natural waters. The large body size (mean total length: 803 mm), pigmented skin, enlarged eyes, and relatively matured gonads (mean gonad somatic index: 1.9) found in non-native European eels indicated that most had metamorphosed into the migratory silver phase, suggesting their ability to initiate spawning migration. However, the proportion of European eels in Mikawa Bay in 1997 was more than 12%, which decreased markedly to less than 2% after 2001, corresponding to the recent decline in import of European glass eels for aquaculture. This suggests that the population of European eels will decrease in Japanese waters in the future.     

Changes in otolith microchemistry of the Japanese eel, Anguitta japonica, during its migration from the ocean to the rivers of Taiwan

The newly recruited Japanese eel, Anguilla japonica , elvers and 1-year-old eels collected in estuaries and in rivers, respectively, were studied. The microstructure and chemical composition of the sagittal otolith of these eels were examined by SEM and wavelength-dispersive spectrometer (WDS), A transition zone or'elver mark'was observed in the otolith of the young eels. A comparison of the otoliths of elvers with those from the 1-year-old eels suggests that this transition zone was deposited during upstream migration, a change from a marine to freshwater environment. Strontium (Sr) content in the primordium of the otolith of both elvers and young eels was low, probably due to the maternal or freshwater origin of the oocyte. The concentration of Sr in the otolith increased gradually during marine life and reached a peak approximately 1 month before upstream migration. As the elvers entered the estuary, the Src concentration dramatically decreased and remained at a low level thereafter. These findings indicate that the history of the migratory environment of the eel can be reconstructed from a combined study of otolith microstructure and microchemistry analysis.     

Evidence of local short‐distance spawning migration of tropical freshwater eels,and implications for the evolution of freshwater eel migration

Freshwater eels have fascinated biologists for centuries due to the spectacular long‐distance migrations between the eels’ freshwater habitats and their spawning areas far out in the ocean and the mysteries of their ecology. The spawning areas of Atlantic eels and Japanese eel were located far offshore in the Atlantic Ocean and the Pacific Ocean, respectively, and their reproduction took place thousands of kilometers away from their growth habitats. Phylogenetic studies have revealed that freshwater eels originated in the Indonesian region. However, remarkably little is known about the life histories of tropical freshwater eels despite the fact that tropical eels are key to understanding the nature of primitive forms of catadromous migration. This study found spawning‐condition tropical freshwater eels in Lake Poso, central Sulawesi, Indonesia, with considerably high gonadosomatic index values and with histologically fully developed gonads. This study provides the first evidence that under certain conditions, freshwater eels have conditions that are immediately able to spawn even in river downstream. The results suggest that, in contrast to the migrations made by the Atlantic and Japanese eels, freshwater eels originally migrated only short distances of <100 kilometers to local spawning areas adjacent to their freshwater growth habitats. Ancestral eels most likely underwent a catadromous migration from local short‐distance movements in tropical coastal waters to the long‐distance migrations characteristic of present‐day temperate eels, which has been well established as occurring in subtropical gyres in both hemispheres.     

Factors determining length distribution and abundance of the European eel, Anguilla anguilla, in the River Mondego (Portugal)

1. The distribution and abundance of the European eel, Anguilla anguilla, were investigated in the Mondego River, a strongly modified river in central Portugal. Nine freshwater sites, located below the first impassable obstacle to eel migration, were surveyed for 2 years. The study was conducted monthly during the first year and seasonally during the second year. Fish were caught by electric fishing and, physical and biotic variables potentially influencing eel length distribution and abundance were determined at each sampling session. 2. Canonical correspondence analysis (CCA) was used to explain the relationships between abiotic and biotic habitat variables, and eel length distribution. Spatial variation was strongly associated with distance from the sea, number of obstacles, river width and percentage of instream cover. Depth, river flow, water temperature and cannibalism had weaker effects on the longitudinal distribution, but contributed as explanatory variables for the model. The influence of spatial variables outweighed the importance of temporal variables as predictors in this model. 3. Length distribution changed in space from a dominance of small eels (<100 mm) closer to the sea to larger eels (≥250 mm) in the upper reaches of the river. The smallest length class (eels <100 mm) was strongly associated with wider stretches where instream cover, mainly composed of aquatic submerged macrophytes, was abundant (>75% area coverage). On the contrary, larger eels (≥250 mm) preferred deeper stretches with stronger river flow and less instream cover. 4. The effect of biotic interactions with conspecifics as well as with the non‐native red swamp crayfish Procambarus clarkii, in sites with poor instream cover, modified this general pattern of distribution leading to fewer eels <100 mm at some sites closer to the sea. Therefore, despite the ubiquity and plasticity shown by this species, there were clear ontogenetic variations in habitat use such that the first two canonical axes of a CCA accounted for 58.4% of the spatial variability in size structure.     

Annual variability in upstream migration of glass eels in a southern USA coastal watershed

We investigated the environmental factors that affected temporal variability of eel recruitment and upstream migration in a freshwater coastal river along the southeastern US. Glass eels Anguilla rostrata were collected through ichthyoplankton sampling in the lower Roanoke River, North Carolina. Monthly samples were taken from fixed stations from May 2001 through June 2003. There was no evidence of consistent seasonal migration patterns for glass eels in Roanoke River. From May through December in 2001, glass eels were captured only during August. In 2002, glass eels arrived in February and remained in ichthyoplankton samples through October, with the exception of samples from September. Peak catch occurred in March at 4.02 ± 1.2 and declined through June to 0.18 ± 0.07 (#/1,000 m³). By August, the mean density increased to 0.96 ± 0.82 and to 3.59 ± 2.77 by October. In 2003 from January through June, glass eels were captured only during February and March. Glass eels were routinely collected when river discharge rates were <150 m³ s⁻¹. River discharge rates >650 m⁻³ s⁻¹ resulted in no glass eels in our samples. Upstream migration during 2002 was not correlated with water temperature or related to lunar phase. Glass eel freshwater upstream migration was initiated when water temperatures exceeded a threshold range of 10°C to 15°C; however, glass eels continued to migrate when water temperatures approached 30°C. The overall negative effect of river discharge suggests that changes in the water release schedules of upstream hydroelectric facilities during glass eel migration could strongly influence their recruitment success.     

Density-dependent and inter-specific interactions affecting European eel settlement in freshwater habitats

Identifying the factors influencing the settlement of European eel (Anguilla anguilla) juveniles in continental habitats is crucial to designing effective management and conservation measures for this endangered species. A long-term data series (1993–2008) of European eel and European catfish (Silurus glanis) abundance in a freshwater canal of the Camargue water system (southern France), along with parallel data on water salinity and glass eel abundance in the adjacent Vaccarès lagoon, was analysed to identify the possible causes of decline in eel abundance observed in the canal during the last two decades. A model including glass eel recruitment and catfish abundance as covariates explained 78% of the observed variation in eel settlement success. Results suggest that (1) salinity does not play a significant role in determining the fraction of eels moving from the brackish lagoon to the canal; (2) density dependence affects settlement success, possibly through a reduction of juvenile survival in the adjacent lagoon; and (3) catfish abundance is negatively correlated with eel settlement. We discuss this latter point in terms of possible predation of catfish upon eels and/or inter-specific competition between the two species.     

Relationships between locomotor behavior, morphometric characters and thyroid hormone levels give evidence of stage-dependent mechanisms in European eel upstream migration

In order to decipher movements during freshwater eel colonization, we experimentally characterized individual locomotor behavior of two eel life history stages: elvers and yellow eels. A ramp located at the flume tank upstream side required a specific locomotor behavior to be ascended. Placing individually tagged eels in the middle of the tank three times successively tested behavioral consistency. Eels climbing the ramp on each trial were classified as "upstream climbers" whereas eels settling in the tank middle were classified as "inactive". Both stages exhibited these two opposite consistent behaviors. However, elvers were predominantly "upstream climbers" (58.1%) whereas yellow eels were predominantly "inactive" (79.6%). We measured morphometric characters and thyroid hormones to determine if upstream activity was related to body condition and thyroid status. Elver upstream climbers had higher body condition as well as higher thyroxine (T(4)) and triiodothyronine (T(3)) levels compared with inactive elvers. Yellow eel upstream climbers had lower body length as well as higher T(3) and (T(3):T(4)) ratio compared with inactive yellow eels. This indicated that the physiological release factors for eel upstream migration may be stage dependent. For elvers, high thyroid gland activity, together with high body condition, may be the physiological release factors for migration. In contrast, for yellow eels, physiological stress may be the release factor with an increase in T(4) deiodination activity in the smallest eels. Our study revealed inter-stage and intra-stage locomotor behavior plasticity and suggested stage-dependent opposite impacts of physiological condition on eel upstream migration.     

A long-term study of population characteristics and downstream migrations of the European eel Anguilla anguilla (L.) and the effects of a migration barrier in the Girnock Burn, north-east Scotland

Downstream migrations and population characteristics of eels Anguilla anguilla were studied between 1967–1982 and 2002–2005 using a fish trap and electrofishing in the Girnock Burn, a small oligotrophic upland sub‐catchment of the River Dee, north‐east Scotland, 70 km from the tidal limit. In limited mark‐recapture studies, 9% of eels were recaptured up to three times and 97% of all recaptures were made at the same electrofishing site. The recaptured eels had a low mean growth rate of c. 13 mm year⁻¹. Smaller eels appeared to show preferences for shallower habitats with small boulder and gravel–sand substrata. Trap catches exhibited seasonal modes in total length at 140–180 mm in late spring, and 320–340 mm in early autumn, probably relating to water temperatures and discharges. From other studies, it is inferred that the spring mode comprised sexually undifferentiated nomadic eels and the autumn mode differentiated males beginning their spawning migration. Large female eels were rare. The fish trap appears to have formed a major barrier to upstream migration since its construction in 1966. In‐stream density has decreased significantly since then from 16 to three eels 100 m⁻², biomass from 260 to 78 g 100 m⁻² and emigrants from 700 to 100 individuals year⁻¹. Emigrants have comprised c. 5% of the standing stock year⁻¹ since the 1970s. The proportion of larger differentiated eels in the Girnock Burn has, however, remained relatively constant and escapement has been c. 100–200 (probably male) eels year⁻¹ since the late 1960s. Evidence, including that from other northerly British rivers, is reviewed to assess the possible impacts of Europe‐wide declines in glass eel recruitment since the 1980s. It is recommended that the data series be maintained, plus further sex determination and ageing studies. Installation of an upstream trap to capture immigrants and studies of recolonization are proposed.     

Role of Eel Odour on the Efficiency of an eel, Anguilla anguilla, Ladder and Trap

The influence of eel odour on the efficiency of a freshwater eel ladder and trap was assessed during two glass eel and yellow eel springtime upstream migration seasons in the Vilaine estuary, France. This test consisted of alternatively directing the outflow from the trap holding bin, away from, or onto the trap access ladder and comparing catches. Catches were 1.4 higher for both glass eels and juvenile eels when the trap water was directed towards the pass. The experiment had little influence on predicting ladder catches when compared to the environmental parameters. The distance of detection of the scent was calculated to range between 0 and 5m from the ladder.     

Hematology patterns of migrating European eels and the role of EVEX virus

We show that European eels infected with the rhabdovirus EVEX (Eel Virus European X) virus, developed hemorrhage and anemia during simulated migration in large swim tunnels, and died after 1000-1500 km. In contrast, virus-negative animals swam 5500 km, the estimated distance to the spawning ground of the European eel in the Sargasso Sea. Virus-positive eels showed a decline in hematocrit, which was related to the swim distance. Virus-negative eels showed a slightly increased hematocrit. Observed changes in plasma lactate dehydrogenase (LDH), total protein and aspartate aminotransferase (AAT) are indicative of a serious viral infection. Based on these observations, we conclude that eel virus infections may adversely affect the spawning migration of eels, and could be a contributing factor to the worldwide decline of eel.     

Environmental cues and extended estuarine residence in seaward migrating eels (Anguilla australis)

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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.     

Silver eel,Anguilla anguilla (Linnaeus, 1758), migration patterns in lowland rivers and lagoons in the North‐Eastern region of their distribution range

Escapement success and migration patterns of silver eels Anguilla anguilla (L.) was studied by acoustic telemetry in three natural free‐flowing and one dammed river and in Curonian Lagoon in Lithuania. Mean downstream migration speed and escapement success were almost the same in the shorter 210 km dammed river (52%, 13.6 km/day) and the considerably longer 300–480 km free‐flowing rivers (53%, 10.7 km/day). Despite the similarity between migration speed in the Curonian Lagoon (14.6 km/day) to that in rivers, migration success was significantly higher (71%) in the Lagoon. Although a majority of silver eels in Lithuania start migrating downstream in spring, the peak of eel migration into the Baltic Sea was observed during late fall. Overall migration success in the rivers and the Lagoon was 35%. Relatively low escapement may have negative consequences on the success on eel stock restoration and must be addressed when strategically planning for the production of spawners.     

Loss of European silver eel passing a hydropower station

The aim of this study was to assess escapement success of silver eels, Anguilla anguilla (L.), in a lowland river while passing a reservoir and a hydropower station. It was hypothesized that passage success would be lowest at the hydropower station and that survival and migration speed would be highest in the free‐flowing river section upstream the reservoir. Forty‐five female silver eels 56–86 cm in length were tagged with acoustic transmitters and released in November 2006. Their migration was monitored via automatic listening stations (ALS) in various sections of the river, covering a total migration distance of 64 km. Survival and progression rate of downstream migration was highest in the upstream river section and significantly lower in the reservoir. The eels apparently had trouble finding their way past the turbines and spent between 1.5 and 35 h in the forebay. The results show that within the study period, only 23% of the tagged eels reached the tidal limit, mainly due to difficulties in passing the hydropower dam. With such high loss‐rates, the escapement goals set in the management plan cannot be achieved.     

The Giant Mottled Eel,Anguilla marmorata,Uses Blue-Shifted Rod Photoreceptors during Upstream Migration

Catadromous fishes migrate between ocean and freshwater during particular phases of their life cycle. The dramatic environmental changes shape their physiological features, e.g. visual sensitivity, olfactory ability, and salinity tolerance. Anguilla marmorata, a catadromous eel, migrates upstream on dark nights, following the lunar cycle. Such behavior may be correlated with ontogenetic changes in sensory systems. Therefore, this study was designed to identify changes in spectral sensitivity and opsin gene expression of A. marmorata during upstream migration. Microspectrophotometry analysis revealed that the tropical eel possesses a duplex retina with rod and cone photoreceptors. The λ_max of rod cells are 493, 489, and 489 nm in glass, yellow, and wild eels, while those of cone cells are 508, and 517 nm in yellow, and wild eels, respectively. Unlike European and American eels, Asian eels exhibited a blue-shifted pattern of rod photoreceptors during upstream migration. Quantitative gene expression analyses of four cloned opsin genes (Rh1f, Rh1d, Rh2, and SWS2) revealed that Rh1f expression is dominant at all three stages, while Rh1d is expressed only in older yellow eel. Furthermore, sequence comparison and protein modeling studies implied that a blue shift in Rh1d opsin may be induced by two known (N83, S292) and four putative (S124, V189, V286, I290) tuning sites adjacent to the retinal binding sites. Finally, expression of blue-shifted Rh1d opsin resulted in a spectral shift in rod photoreceptors. Our observations indicate that the giant mottled eel is color-blind, and its blue-shifted scotopic vision may influence its upstream migration behavior and habitat choice.