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.     

Recruitment abundance estimation: Role of glass eel (Anguilla anguilla L.) response to light

Most fish populations are declining worldwide and their management would benefit from a better estimation of recruitment. In glass eels, field studies suggest that estuarine migratory glass eels are sensitive enough to light to change their vertical location according to factors such as water turbidity and/or moon brightness. The response of glass eel (Anguilla anguilla L.) to light was tested in the laboratory using boxes where fish could choose between a lit and an unlit side. Responses were quantified as the proportion of glass eels remaining in the unlit chamber. Decreasing light levels were used and tested on different “age” glass eels (“age” in days since capture). In addition, measures of light at different depths of the water column were carried out in the Adour estuary (43°30′ N, 1°30′ W). The glass eel light avoidance level was lower in non-pigmented glass eel (less than 10 ^− 10 W cm ^− 2), than in pigmented ones (10 ⁻⁹-10 ^− 8 W cm ^− 2). These results and field data on the measurement of light energy in the water column of Adour estuary are compared with previously published data on the estuarine migration of glass eel.     

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.     

Flow-carried and active swimming migration of the glass eel(Anguilla anguilla) in the tidal area of a small estuary on the French Atlantic coast

The study of the migration dynamics of glass eels(Anguilla anguilla) in a small estuary of the French Atlantic coast shows a two-stage sequence: (1) From November to March, the glass eels migrate upstream by using the tidal currents. The estuarine hydrology leads to a natural trapping of migrants in a typical area where the current speed slows down. The location of this zone depends on hydraulic conditions. The greater the tide is the farther upstream this area will be. This phenomenon leads to an increasing catchability of elvers. (2) From April onwards, when the water temperature reaches 10–12 °C, the glass eels swim actively upstream in the estuary. Then, fish concentrate just below the first dam. This behaviour shift shows the beginning of the colonization process of the whole riverine system.     

The effect of salinity on the chemotaxis of glass eels, Anguilla anguilla, to organic earthy and green odorants

Synopsis The behaviour of upstream migrating glass eels to salt and brackish water solutions of 8 pure organic earthy and green odorants was investigated. In 35 salt water, IPMCET and D-MF are ineffective, while MMP, IBMP, MT, TMCE, ETMCE and L-MF are strongly repellent. Dissolved in brackish water, MMP and ETMCE become attractive. The strong attraction which glass eels show to earthy and green odorants emerges as the level of salinity is reduced, suggesting that these chemicals could be orienting cues in the last phase of glass eel migration.     

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.     

Optimizing the mass marking of fish with alizarin red S: an example with glass eels

Fish marking is an essential tool for fisheries management, especially for evaluating the stocking of endangered fish species to support conservation and sustainable use of fish stocks. Batch marking of young European eels Anguilla anguilla (L.) prior to stocking is recommended as the benefits of stocking for the spawning stock can be evaluated by recapturing marked fish over time, therefore mass marking of young eels with substances such as alizarin red S (ARS) is becoming increasingly important. To improve the marking method and reduce marking costs when immersing glass eels in an ARS solution, eight laboratory experiments under varying conditions (e.g., temperature, ARS concentration, immersion time, osmotic induction, fish density) and with ARS from different suppliers were carried out. The results show that optimal marking of glass eels can be carried out in the field or during transport by putting approximately 50 g of glass eels per liter in 150 mg L⁻¹ ARS solution for 3 h at 10–15°C. Lower concentrations did not result in reliable marking. Water temperatures of 5°C and below can have a stunning effect on the eels and increase mortality significantly, regardless of the concentration of ARS. Glass eel densities below 50 g L⁻¹ in the marking bath increase marking costs unnecessarily, while a higher density of 100 g L⁻¹ resulted in significantly higher mortality and lower marking success. A somewhat more difficult but less expensive alternative is to bathe the fish in a saline solution of 1% (10 PSU) of 80 mg L⁻¹ ARS for 3 h at 10°C. Costs can also be significantly reduced by choice of supplier for ARS, but care should be taken as the quality of the powder appears to vary (mean percentage of sufficiently marked eels ranged from 59% to 91% among suppliers in the present study) and can lead to marking failure. The optimal marking conditions can help ensure that stocked glass eels can be reliably identified in future studies to assess stocking benefits while reducing costs.     

Water temperature and upstream migration of glass eels in New Zealand: implications of climate change

Glass eels migrating upstream in a New Zealand river showed a clear preference for water temperatures between 12 and 20°C, with an optimum of 16.5°C. Water temperatures <12°C and >22°C almost completely inhibited migration, which implies that warmer temperatures associated with global climate change might have a detrimental impact on glass eel recruitment in their current ranges. We established this by trapping glass eels of shortfin, Anguilla australis, and longfin, A. dieffenbachii, eels nightly from September to November. Eels caught in 2001 (50,287) outnumbered those caught in 2002 (19,954); shortfin glass eels dominated catches in both years, comprising 91–93% of the catch. Longfins were larger than shortfins, and size and pigmentation in both species increased as the seasons progressed. Temperatures within the migratory season in 2001 showed ∼14-day intervals between maxima that appeared to be associated with the new and full moons.     

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.     

Effects of body condition and water temperature on Anguilla anguilla glass eel migratory behavior

Glass eels arriving from the sea use alternative migratory tactics, leading either to the colonization of rivers or to an early settlement in marine or estuarine habitats. In the field, the migration may be environmentally affected by water temperature and the migratory behavior could be physiologically dependent on the body condition (energetic status). To investigate how these environmental and physiological effects on the migration are behaviorally mediated, we experimentally tested the effects of changes in water temperature and body condition on locomotor activity (upstream swimming) and salinity preference of Anguilla anguilla glass eels. Low water temperature reduced significantly both locomotor activity and preference for freshwater, in accordance with field data showing that low water temperatures hinder both the estuarine migration and river recruitment. Glass eels switched from a freshwater- towards a saltwater-preference as their body condition decreased, confirming that the energetic status may affect the migratory behavior. We suggest that, in the wild, this condition-dependent change in salinity preference of low body condition glass eels induces an early settlement in marine or estuarine habitats. Such a behavioral shift, stopping the energy expenditure linked to river-oriented migratory behavior, may be adaptive by limiting the probability of death due to exhaustion. Our results show that the glass eel migratory behavior, through locomotor activity and salinity preference, may be controlled by interacting physiological and environmental factors.     

Application of otolith microchemistry to estimate the migratory history of Japanese eel Anguilla japonica on the Sanriku Coast of Japan

The age and migratory history of the Japanese eel, Anguilla japonica Temminck & Schlegel, collected in Miyako Bay along the Sanriku coast of Japan, was examined using the otolith microstructure and analysis of strontium (Sr) and calcium (Ca) concentrations conducted with wavelength dispersive X‐ray spectrometry by an electron microprobe. The line analysis of Sr : Ca ratios along the life history transect of each otolith showed a peak (ca. 15–17 × 10^?3) which corresponded with the period of their leptocephalus and early glass eel stages in the ocean. The mean Sr : Ca ratios from the elver mark to the otolith edge indicated that there were eels with several general categories of migratory history, including sea eels that never entered freshwater (average Sr : Ca ratios, ≥6.0 × 10^?3), and others that entered freshwater for brief periods but returned to the estuary or bay. This evidence of the occurrence of sea eels in this northern area indicates that Japanese eels of the Sanriku coast do not necessarily migrate into freshwater rivers during recruitment as do glass eels at the beginning of their growth phase; even those that do enter freshwater may later return to the marine environment. Thus, anguillid eel migrations into freshwater are clearly not an obligatory migratory pathway, but rather a facultative catadromy with seawater or estuarine residents as an ecophenotype.     

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.     

Interspecific and sexual differences in riverine distribution of tropical eels Anguilla spp.

A total of 261 individuals of the four tropical eel species, Anguilla celebesensis, Anguilla marmorata, Anguilla bicolor pacifica and Anguilla interioris, were collected from 12 locations around Sulawesi Island, Indonesia, to gain knowledge about the riverine distribution of tropical eels. Anguilla marmorata was predominant in the lower reaches of Poso River (94·4% of total eel catch in the sampling area), Poso Lake (93·3%), three small inlet rivers of Tomini Bay (100%) and Laa River (92·3%). Anguilla celebesensis occurred frequently in the inlet rivers of Poso Lake (63·5%). Anguilla bicolor pacifica and Anguilla interioris were rare (1.5 and 0.4%, respectively). Otolith Sr:Ca ratio electron‐probe micro analysis (EPMA) for individual migratory histories revealed that 15 A. celebesensis caught in Poso Lake and its inlet rivers were categorized into 14 river eels (Sr:Ca < 2·5) showing upstream migration seemingly at their elver stage and only one sea eel (Sr:Ca ≥ 6·0) that stayed in the marine habitat for the majority of its life after recruiting to Sulawesi Island before its late upstream migration. In A. marmorata, 19 examined eels from Poso Lake and its inlet rivers were all river eels, while 17 eels from the lower reaches of Poso River were two river eels, six sea eels and nine estuarine eels (2·5 ≤ Sr:Ca < 6·0) that mostly lived in the brackish water. The sex ratio of A. celebesensis was highly skewed towards a dominance of females (99%). In A. marmorata, females were predominant in Poso Lake (95·2%), its inlet rivers (94·7%) and Laa River (100%), while males were more frequent in the lower reaches of Poso River (76·5%) and small inlet rivers of Tomini Bay (94·1%). These results indicate that the riverine distribution pattern of tropical eels differs among species and between sexes.     

Individual patterns of rhythmic swimming activity in Anguilla anguilla glass eels synchronised to water current reversal

The existence of distinct patterns of activity and swimming behaviour were tested in individual European glass eels by means of Bayesian inference mixture modelling. 36 glass eels were tagged using Visible Implant Elastomer and added to 36 untagged glass eels in February and April. Each group was presented with a change in water current direction every 6,2 h and videotaped during 2 weeks. Two hypotheses were tested: (i) all individuals display a similar pattern of behaviour within a tidal period, glass eels showing both positive and negative rheotaxis in opposite phase (M1 model) and (ii) individuals are distributed in two different groups, some glass eels swimming with and the others against the current (M2 model). Results showed that most glass eels displayed a positive or a negative rheotaxis and only a small number exhibited both behaviours. All swimming behaviours were synchronised to a change in current direction with a period close to the tidal one. Results are discussed in relation to synchronisation and migration behaviour.     

Signatures of natural selection between life cycle stages separated by metamorphosis in European eel

Background

Species showing complex life cycles provide excellent opportunities to study the genetic associations between life cycle stages, as selective pressures may differ before and after metamorphosis. The European eel presents a complex life cycle with two metamorphoses, a first metamorphosis from larvae into glass eels (juvenile stage) and a second metamorphosis into silver eels (adult stage). We tested the hypothesis that different genes and gene pathways will be under selection at different life stages when comparing the genetic associations between glass eels and silver eels.

Results

We used two sets of markers to test for selection: first, we genotyped individuals using a panel of 80 coding-gene single nucleotide polymorphisms (SNPs) developed in American eel; second, we investigated selection at the genome level using a total of 153,423 RAD-sequencing generated SNPs widely distributed across the genome. Using the RAD approach, outlier tests identified a total of 2413 (1.57 %) potentially selected SNPs. Functional annotation analysis identified signal transduction pathways as the most over-represented group of genes, including MAPK/Erk signalling, calcium signalling and GnRH (gonadotropin-releasing hormone) signalling. Many of the over-represented pathways were related to growth, while others could result from the different conditions that eels inhabit during their life cycle.

Conclusions

The observation of different genes and gene pathways under selection when comparing glass eels vs. silver eels supports the adaptive decoupling hypothesis for the benefits of metamorphosis. Partitioning the life cycle into discrete morphological phases may be overall beneficial since it allows the different life stages to respond independently to their unique selection pressures. This might translate into a more effective use of food and niche resources and/or performance of phase-specific tasks (e.g. feeding in the case of glass eels, migrating and reproducing in the case of silver eels).

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1754-3) contains supplementary material, which is available to authorized users.     

Migratory history and habitat use by New Zealand freshwater eels <Emphasis Type="Italic">Anguilla dieffenbachii</Emphasis> and <Emphasis Type="Italic">A. australis</Emphasis>, as revealed by otolith microchemistry

 The migratory history of Anguilla dieffenbachii and A. australis, collected from a coastal lake of New Zealand, was examined using analysis of strontium (Sr) and calcium (Ca) concentrations. Line analysis of Sr : Ca ratios along the life history transect of each otolith showed a peak (Ca. 16–20 × 10⁻³) between the core and elver mark, which corresponded to the period of their leptocephalus and early glass eel stages in the ocean. The mean Sr : Ca ratios from the elver mark to the otolith edge indicated that eels had different migratory histories, which included freshwater residency in some eels (average Sr : Ca ratios, 1.7 × 10⁻³–2.4 × 10⁻³) but not in others (average Sr : Ca ratios, 3.1 × 10⁻³–6.5 × 10⁻³). These findings suggest that New Zealand freshwater eels have a flexible migration strategy and an ability to adapt to various habitats and salinities. Received: November 25, 2002 / Revised: January 17, 2003 / Accepted: January 17, 2003     

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.     

Growth and Production of Yellow Eels and Glass Eels in Ponds

Two experiments (I and II) were performed in drainable ponds. Yellow eels Anguilla anguilla (L.) were stocked in early June at three biomasses: 10, 20 and 60 kg · ha⁻¹ in experiment I; and 10, 20 and 40 kg · ha⁻¹ in experiment II. The mean body weights were 27.0 and 24.2 g respectively. Glass eels were stocked only in experiment II at equal densities of 1600·ha⁻¹. In both experiments each biomass of yellow eel was combined in a factorial design with three cyprinid communities differing in biomass and in species- and size-composition. The ponds were drained in autumn. The final body weights at draining ranged from 25.9 to 63.6 g for yellow eel and from 3.9 to 8.8 g for glass eel. The final body weights of yellow eel and of glass eel decreased with increasing biomass of yellow eel. No significant relation was found between the bream Abramis brama (L.) biomass and the growth of eel. The growth rates of yellow eel and glass eel were positively correlated in experiment II. At higher biomasses of yellow eel the percentage females decreased slightly. The recapture rates of yellow eel in experiments I and II amounted to 69.4 ± 9.8 % and 92.2 ± 4.9% (mean ± sd) respectively. The lower recapture rates in experiment I were caused by the inappropriate draining technique used. The glass eels were recaptured with 75.0·5.6% efficiency. The maximum net production of yellow eel occurred at a biomass of 20–40kg·ha⁻¹ and amounted to 19 kg·ha⁻¹.     

Bile salts and taurine as chemical stimuli for glass eels,Anguilla anguilla: a behavioural study

Synopsis The behaviour of migrating glass eels towards different concentrations of seven bile salts and taurine was investigated by binary-choice experiments. All substances attracted glass eels when presented at concentrations below 10^–10M. Glycocholate, taurodeoxycholate and taurine remained attractive at higher concentrations, while taurocholate, cholate, deoxycholate, glycochenodeoxycholate and taurochenodeoxycholate became repellent. A role of bile salts in grouping and orientation behaviour of glass eels is discussed.