Influence of oceanic factors on Anguilla anguilla (L.) over the twentieth century in coastal habitats of the Skagerrak,southern Norway

The European eel (Anguilla anguilla L.) is distributed in coastal and inland habitats all over Europe, but spawns in the Sargasso Sea and is thus affected by both continental and oceanic factors. Since the 1980s a steady decline has been observed in the recruitment of glass eels to freshwater and in total eel landings. The eel is considered as critically endangered on the International Union for the Conservation of Nature and Natural Resources Red List of species. The Skagerrak beach seine survey from Norway constitutes the longest fishery-independent dataset on yellow/silver eels (starting in 1904). The Skagerrak coastal region receives larvae born in the Sargasso Sea spawning areas that have followed the Gulf Stream/North Atlantic Drift before they penetrate far into the North Sea. The Skagerrak coastal time series is therefore particularly valuable for exploring the impacts of oceanic factors on fluctuations in eel recruitment abundance. Analyses showed that Sargasso Sea surface temperature was negatively correlated with eel abundance, with a lag of 12 years revealing a cyclic and detrimental effect of high temperatures on the newly hatched larvae. The North Atlantic Oscillation index and inflow of North Atlantic water into the North Sea were negatively correlated with eel abundance, with a lag of 11 years. Increased currents towards the North Atlantic during high North Atlantic Oscillation years may send larvae into the subpolar gyre before they are ready to metamorphose and settle, resulting in low recruitment in the northern part of the distribution area for these years. The Skagerrak time series was compared with glass eel recruitment to freshwater in the Netherlands (Den Oever glass eel time series), and similar patterns were found revealing a cycle linked to changes in oceanic factors affecting glass eel recruitment. The recent decline of eels in the Skagerrak also coincided with previously documented shifts in environmental conditions of the North Sea ecosystem.     

A global viability assessment of the European eel

The global European eel (Anguilla anguilla) stock is critically endangered according to the IUCN, and the European Commission has urged the development of conservation plans aimed to ensure its viability. However, the complex life cycle of this panmictic species, which reproduces in the open ocean but spends most of its prereproductive life in continental waters (thus embracing a huge geographic range and a variety of habitat types), makes it difficult to assess the long‐term effectiveness of conservation measures. The interplay between local and global stressors raises intriguing cross‐scale conservation challenges that require a comprehensive modelling approach to be addressed. We developed a full life cycle model of the global European eel stock, encompassing both the oceanic and the continental phases of eel's life, and explicitly allowing for spatial heterogeneity in vital rates, availability of suitable habitat and settlement potential via a metapopulation approach. We calibrated the model against a long‐term time series of global European eel catches and used it to hindcast the dynamics of the stock in the past and project it over the 21st century under different management scenarios. Although our analysis relies on a number of inevitable simplifying assumptions and on data that may not embrace the whole range of variation in population dynamics at the small spatiotemporal scale, our hindcast is consistent with the general pattern of decline of the stock over recent decades. The results of our projections suggest that (i) habitat loss played a major role in the European eel decline; (ii) the viability of the global stock is at risk if appropriate protection measures are not implemented; (iii) the recovery of spawner escapement requires that fishing mortality is significantly reduced; and (iv) the recovery of recruitment might not be feasible if reproductive output is not enhanced.     

Recruitment of Anguilla spp. glass eels in the Waikato River,New Zealand. Evidence of declining migrations?

The timing of Anguilla spp. glass eel recruitment into the Waikato River, North Island, New Zealand, was studied over a 2 year period (2004–2005). While glass eels of both the shortfin eel Anguilla australis and the endemic longfin eel Anguilla dieffenbachii were caught, the former comprised >97% of the species composition. There was a positive correlation of glass eel migrations with spring tides, with peak migration periods typically occurring within a few hours of the peak of high tide, and between 2 and 4 days after the day of spring tide. Both water temperature and discharge had significant inverse relationships with glass eel catches, with temperature explaining >30% of the variance in catch periodicity. Comparison of catch data 30 years apart showed that main migration periods appear to occur several weeks earlier today than previously. Reduced catch per unit effort and duration of runs from recent years' sampling (compared with the 1970s) indicate that a reduction in recruitment may also have occurred during this period, something recorded in other temperate species of Anguilla .     

Oceanic fronts in the Sargasso Sea control the early life and drift of Atlantic eels

Anguillid freshwater eels show remarkable life histories. In the Atlantic, the European eel (Anguilla anguilla) and American eel (Anguilla rostrata) undertake extensive migrations to spawn in the oceanic Sargasso Sea, and subsequently the offspring drift to foraging areas in Europe and North America, first as leaf-like leptocephali larvae that later metamorphose into glass eels. Since recruitment of European and American glass eels has declined drastically during past decades, there is a strong demand for further understanding of the early, oceanic phase of their life cycle. Consequently, during a field expedition to the eel spawning sites in the Sargasso Sea, we carried out a wide range of dedicated bio-physical studies across areas of eel larval distribution. Our findings suggest a key role of oceanic frontal processes, retaining eel larvae within a zone of enhanced feeding conditions and steering their drift. The majority of the more westerly distributed American eel larvae are likely to follow a westerly/northerly drift route entrained in the Antilles/Florida Currents. European eel larvae are generally believed to initially follow the same route, but their more easterly distribution close to the eastward flowing Subtropical Counter Current indicates that these larvae could follow a shorter, eastward route towards the Azores and Europe. The findings emphasize the significance of oceanic physical–biological linkages in the life-cycle completion of Atlantic eels.     

Assessment of the environmental drivers of European glass eel (Anguilla anguilla) recruitment in transitional waters

The European eel (Anguilla anguilla) has undergone an unprecedented population decline since the 1980s, with current recruitment levels fluctuating from 3 to 15% of historical levels for the last 20 years. Monitoring of glass eels and elvers as 0?+?recruitment is an essential step in helping to understand the trend in recruitment and to better quantify the current recruitment time series. Two locations within the Shannon estuary on the west coast of Ireland were monitored for glass eel recruitment from January to April in 2017 and 2018. This study used a generalised linear mixed model to examine a range of environmental variables impacting on glass eel abundance in transitional waters. Results found that water temperature and moon phase were the most important variables. Tidal height and cloud cover also influenced the abundance of glass eels but to a lesser extent. This study found that focussing survey efforts on nights around the full moon when water temperatures exceed 5℃ will allow a catch which is representative of the population in an estuary. Glass eel monitoring needs a long-term sampling plan in order to account for annual fluctuations apparent in glass eel recruitment.

     

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.     

Distribution of genetic variation in farmed and natural stocks of european eel

European eel ( Anguilla anguilla ; Teleostei) is a valuable commercial species. However, over the past 25 years, the population of European eel has been declining to such a degree that major concerns have been raised for its long‐term conservation. Since little information is available on the life‐cycle and genetic structure of European eel, it has been difficult to evaluate the existence of any population substructuring. Molecular genetic methods contribute to a better knowledge of the demography and population structure in marine fish. In addition, management strategies and conservation goals must consider information on genetic substructuring as well as on life history patterns.
The aim of the study is to provide more detailed knowledge on the genetic variability, demography and population substructuring of European eel by analysing and comparing natural and farmed individuals. Natural eel samples have been obtained in two geographical sites (Netherlands, France) including temporal samples in a short‐scale (within years) and a long‐scale (between years). Simultaneously, farmed glass eels have been grown in two separate batches during one year. Batches have been monitored and genetic samples have been obtained during the year.
A combination of selection‐sensitive (allozymes) and selection‐neutral markers (microsatellites) has been used in the study since selection seems to play an important role in the determination of the quality of future eel spawners. Results suggest a positive correlation between growth and genetic variability since individuals attaining a large length and mass present significant higher heterozygosities.     

American eels produce and release bile acid profiles that vary across life stage

The American eel (Anguilla rostrata) is an imperilled fish hypothesized to use conspecific cues, in part, to coordinate long-distance migration during their multistage life history. Here, holding water and tissue from multiple American eel life stages was collected and analysed for the presence, profile and concentration of bile acids. Distinct bile acid profiles were identified in glass, elver, yellow eel and silver eel holding waters using ultraperformance liquid chromatography high-resolution mass spectrometry and principal component analysis. Taurochenodeoxycholic acid, taurodeoxycholic acid, cholic acid, deoxycholic acid, taurolithocholic acid and taurocholic acid were detected in whole tissue of American glass eels and elvers, and in liver, intestine and gallbladder samples of late-stage yellow eels. Bile acids were not a major component of silver eel washings or tissue. This study is novel because little was previously known about bile acids produced and emitted into the environment by American eels. Future behavioural studies could evaluate whether any bile acids produced by American eels influence conspecific migratory behaviour.     

Factors affecting recruitment of glass eels into the Grey River, New Zealand

The arrival pattern of glass eels of the shortfin eel Anguilla australis and longfin eel Anguilla dieffenbachii was studied over a two successive migration seasons in the Grey River, South Island, New Zealand. Fishing was carried out on selected nights during September to November, for 3 h per night during 2000 and 2001. The number of shortfin glass eels exceeded longfins in both years; earliest glass eels (September) were larger than later glass eels (November), and longfins larger than shortfins, but there were significant differences in size between years for both species. Environmental variables affecting recruitment differed between years, but common variables for both years were sampling date, time after high tide (incoming tide preferred), time after sunset and moon phase; the influence of moon phase appeared to be expressed both through tides (spring tides preferred) and moonlight. During the year of higher discharge variability, both increasing discharge and increased turbidity were also important.     

Seasonal and long-term changes in biometrics of eel larvae: a possible relationship between recruitment variation and North Atlantic ecosystem productivity

The European eel larval life has two stages: the oceanic leptocephalus, in which growth is dependent on food supply, and the metamorphosis glass eel stage, in which feeding and growth are stopped until immigration in estuarine waters. Data from fisheries and experimental surveys in European estuaries at different periods between the 1930s and the 1990s showed a simultaneous decrease of mean length and abundance level. A monthly survey at the Vilaine estuary (Bay of Biscay) during 2 years provided a periodical model of seasonal variation in length and weight of newly recruited glass eels. Otolith microstructure was used to back-calculate larval stage durations and the timing of transatlantic migration. Glass eels entering the estuary in autumn are longer and more numerous than those arriving in summer. They migrated across the ocean during spring and summer, seasons when plankton production is likely to reach maximum levels. The proposed hypothesis regarding the determinism of recruitment in the eel, on the seasonal and on the yearly range, is that leptocephalus growth and glass eel survival are partly dependent on the plankton production at the oceanic scale. Eel recruitment dynamics could provide an integrated figure of large-scale environment fluctuations.     

Anguilla rostrata glass eel ingress into two, U.S. east coast estuaries: patterns, processes and implications for adult abundance

A time series of American eel Anguilla rostrata glass eel abundance, timing and size from Little Egg Inlet, New Jersey (16 years) and Beaufort Inlet, North Carolina (18 years) was used to provide a better understanding of ingress patterns at two, U.S. east coast estuaries. There was no evidence of synchronous declines in abundance between the two locations; however, at the Little Egg Inlet site, glass eels arrived later in the season and at significantly smaller sizes over the duration of the series. One significant linkage between sites was revealed: abundance was positively correlated with winter precipitation. Precipitation differed between sites annually and was correlated with El Niño at Beaufort Inlet and, to a lesser extent, the North Atlantic Oscillation at Little Egg Inlet. It is hypothesized that glass eels may use freshwater signals to enhance recruitment to local estuaries, thus influencing year-class strength, yet the relationship between year-class strength and adult abundance remains unresolved.     

Inter and intra-estuary variability in ingress, condition and settlement of the American eel Anguilla rostrata: implications for estimating and understanding recruitment

The objective of this study was to quantify spatial and temporal variability of anguillid glass eel ingress within and between adjacent watersheds in order to help illuminate the mechanisms moderating annual recruitment. Because single fixed locations are often used to assess annual recruitment, the intra-annual dynamics of ingress across multiple sites often remains unresolved. To address this question, plankton nets and eel collectors were deployed weekly to synoptically quantify early stage Anguilla rostrata abundance at 12 sites across two New Jersey estuaries over an ingress season. Numbers of early-stage glass eels collected at the inlet mouths were moderately variable within and between estuaries over time and showed evidence for weak lunar phase and water temperature correlations. The relative condition of glass eels, although highly variable, declined significantly over the ingress season and indicated a tendency for lower condition A. rostrata to colonize sites in the lower estuary. Accumulations of glass eels and early-stage elvers retrieved from collectors (one to >1500 A. rostrata per collector) at lower estuary sites were highly variable over time, producing only weak correlations between estuaries. By way of contrast, development into late-stage elvers, coupled with the large-scale colonization of up-river sites, was highly synchronized between and within estuaries and contingent on water temperatures reaching c. 10−12° C. Averaged over the ingress season, abundance estimates were remarkably consistent between paired sites across estuaries, indicating a low degree of interestuary variability. Within an estuary, however, abundance estimates varied considerably depending on location. These results and methodology have important implications for the planning and interpretation of early-stage anguillid eel surveys as well as the understanding of the dynamic nature of ingress and the spatial scales over which recruitment varies.     

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.     

Head shape dimorphism in European glass eels (Anguilla anguilla)

The life cycle of the European eel (Anguilla anguilla) remained a mystery until the 20th century, when Schmidt discovered that the Sargasso Sea was its spawning area. However, many aspects of the eel's life cycle remain poorly understood. Among these is the bimodal distribution in head shape, with broad- and narrowheaded phenotypes reported in the yellow eel stage. Although this has been linked to dietary preferences of the yellow eels, very little is known about why, how and when this dimorphism arises during their ontogeny. To determine whether this dimorphism indeed appears in relation to trophic niche segregation, we examined head shape variation at an earlier ontogenetic stage, the glass eel stage, as at this stage eels are considered to be non-feeding. Head shape was studied in a large dataset, containing glass eels captured from the Yser river mouth, the Leopold Canal (Belgium) and from the rivers Severn, Trent and Parret (UK), by both taking measurements (head width/head length) and using an outline analysis. Our results show that there is already considerable variation in broadness and bluntness of the head at the glass eel stage. In most cases, equal support for a unimodal and bimodal head shape distribution is found, whereas some cases support head shape bimodality in glass eels, suggesting that glass eel head shape might be shifting from a unimodal to a bimodal distribution. This, in combination with the observation that variation in head width/head length ratios in non-feeding glass eels shows a similar range as in feeding yellow eels, indicates that head shape in European eel might be at least partially determined through other mechanisms than trophic segregation.     

Response of seaward-migrating European eel (Anguilla anguilla) to manipulated flow fields

Anthropogenic structures (e.g. weirs and dams) fragment river networks and restrict the movement of migratory fish. Poor understanding of behavioural response to hydrodynamic cues at structures currently limits the development of effective barrier mitigation measures. This study aimed to assess the effect of flow constriction and associated flow patterns on eel behaviour during downstream migration. In a field experiment, we tracked the movements of 40 tagged adult European eels (Anguilla anguilla) through the forebay of a redundant hydropower intake under two manipulated hydrodynamic treatments. Interrogation of fish trajectories in relation to measured and modelled water velocities provided new insights into behaviour, fundamental for developing passage technologies for this endangered species. Eels rarely followed direct routes through the site. Initially, fish aligned with streamlines near the channel banks and approached the intake semi-passively. A switch to more energetically costly avoidance behaviours occurred on encountering constricted flow, prior to physical contact with structures. Under high water velocity gradients, fish then tended to escape rapidly back upstream, whereas exploratory ‘search’ behaviour was common when acceleration was low. This study highlights the importance of hydrodynamics in informing eel behaviour. This offers potential to develop behavioural guidance, improve fish passage solutions and enhance traditional physical screening.     

Decline of North Atlantic eels: a fatal synergy?

Panmictic species pose particular problems for conservation because their welfare can be addressed effectively only on a global scale. We recently documented by means of microsatellite analysis that the European eel (Anguilla anguilla) is not panmictic but instead shows genetic isolation by distance. In this study, we extended the analysis to the American eel (A. rostrata) by applying identical analytical procedures and statistical power. Results obtained for the American eel were in sharp contrast with those obtained for the European eel: the null hypothesis of panmixia could not be rejected, and no isolation by distance was detected. This implies that the species must be managed as a single population. Using Bayesian statistics, we also found that the effective population sizes for both species were surprisingly low and that the populations had undergone severe contractions, most probably during the Wisconsinan glaciation. The apparent sensitivity of eels to climatic changes affecting the strength and position of the Gulf Stream 20,000 years ago is particularly worrying, given the effects of the ongoing global warming on the North Atlantic climate. Moreover, additional short-term stresses such as surging glass eel prizes, overfishing and lethal parasitic infections negatively affect eel population size. The fascinating transatlantic migration and life cycle of Atlantic eels is also their Achilles' heel as these negative short- and long-term effects will probably culminate in a fatal synergy if drastic conservation measures are not implemented to protect these international biological resources.     

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.     

Qualitative assessment of the diet of European eel larvae in the Sargasso Sea resolved by DNA barcoding

European eels (Anguilla anguilla) undertake spawning migrations of more than 5000 km from continental Europe and North Africa to frontal zones in the Sargasso Sea. Subsequently, the larval offspring are advected by large-scale eastward ocean currents towards continental waters. However, the Sargasso Sea is oligotrophic, with generally low plankton biomass, and the feeding biology of eel larvae has so far remained a mystery, hampering understanding of this peculiar life history. DNA barcoding of gut contents of 61 genetically identified A. anguilla larvae caught in the Sargasso Sea showed that even the smallest larvae feed on a striking variety of plankton organisms, and that gelatinous zooplankton is of fundamental dietary importance. Hence, the specific plankton composition seems essential for eel larval feeding and growth, suggesting a linkage between eel survival and regional plankton productivity. These novel insights into the prey of Atlantic eels may furthermore facilitate eel larval rearing in aquaculture, which ultimately may replace the unsustainable use of wild-caught glass eels.     

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.     

Biochemical and genetic characterization of European silver eels,Anguilla anguilla (Linnaeus, 1758), from the Comacchio lagoon (Italy)

The European eel Anguilla anguilla has declined significantly over recent decades, exceeding its safe biological limits and probably reaching a historical minimum (1% of the 1960 recruitment level). Twenty‐three migrating females at the IV stage of silvering were collected from the Comacchio lagoon (Northern Italy); they showed high levels of cholesterol and triglycerides, probably due to lipid accumulation before migration across the Atlantic Ocean. Electrophoretic patterns showed high amounts of putative α and β globulins, probably due to high concentrations of lipoproteins. Genetic results obtained from a total of 49 specimens (20 from the Comacchio lagoon and 29 from Val Dogà) agree with the panmixia hypothesis, lacking any genetic differentiation over time and space at neutral loci. In conclusion, despite the small sampling and the population decline in recent years, high levels of variability were recorded.