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.     

Rhythmic swimming activity in Anguilla anguilla glass eels: Synchronisation to water current reversal under laboratory conditions

Synchronisation of swimming activity to water current reversal every 6.2 h was tested in the European glass eel (Anguilla anguilla L.). When presented with a change in water current direction, glass eels exhibited rhythmic patterns of activity with a period close to the tidal one. Glass eels began to swim with the current and then alternated between positive and negative rheotaxis after each change in the water current direction. Results are discussed in relation to the flood tidal transport theory. Following synchronisation to current reversal, glass eels subjected to constant conditions displayed a weak rhythmic activity suggesting that locomotor behaviour might, in the wild, synchronise to several environmental cues related to the tide. Results obtained with different densities also suggest that social cues might improve the synchronisation.     

Replication banding in the chromosomes of the European eel (Anguilla anguilla)

The chromosomes of the European eel Anguilla anguilla have been analyzed with a replication banding technique from lymphocyte cultures treated with 5-BrdU. This technique allows us to identify with high resolution the individual chromosome pairs and to differentiate classes of chromatin by the order of replication. The replication banding obtained on the chromosomes of European eel can be related with the structural bands described in this species.     

Cholinesterase activities and sensitivity to pesticides in different tissues of silver European eel, Anguilla anguilla

Cholinesterase (ChE) activities were characterized in silver European eel, Anguilla anguilla, grown in the brackish lagoon of Comacchio (Italy). All specimens were harvested at the “lavoriero”, a traditional eel trapping weir that captures eels while leaving internal waters at the onset of reproductive migration. To our knowledge, no investigation on ChE was reported in silver eels. Therefore a first characterization of enzyme activity in muscle, brain, liver and plasma of silver eel was carried out, in the presence of different substrates, selective inhibitors, and four pesticides representative of the carbamate and organophosphate classes. Brain and white skeletal muscle showed similar ChE activities, 5- and 10-fold higher than those detected in liver and plasma, respectively. Km values of 0.31 and 0.30 mM, and Vmax values of 40.28 and 35.47 nmol min^–1 mg protein^–1 were obtained in brain and muscle ChE, respectively. Acetycholinesterase was the predominant ChE form in all tissues, as concluded by comparing the effects of BW 284c51, iso-OMPA and eserine. ChE activities in brain and muscle were significantly inhibited by in vitro treatment with pesticides, with the following order of potency: carbofuran > carbaryl > chlorpyrifos ≥ diazinon.     

Lectinochemical studies on the affinity of Anguilla anguilla agglutinin for mammalian glycotopes

Anguilla anguilla agglutinin (AAA) is a fucose-specific lectin found in the serum of the fresh water eel. It is suggested to be associated with innate immunity by recognizing disease-associated cell surface glycans, and has been widely used as a reagent in hematology and glycobiology. In order to gain a better understanding of AAA for further applications, it is necessary to elucidate its binding profile with mammalian glycotopes. We, therefore, analyzed the detailed carbohydrate specificity of AAA by enzyme-linked lectinosorbent assay (ELLSA) with our extended glycan/ligand collection and lectin-glycan inhibition assay. Among the glycans tested, AAA reacted well with nearly all human blood group Ah (GalNAcalpha1-->3[LFucalpha1-->2]Gal), Bh (Galalpha1-->3[LFucalpha1-->2]Gal), H LFucalpha1-->2Gal) and Leb (Fucalpha1-->2Galbeta1-->3[Fucalpha1-->4]GlcNAc) active glycoproteins (gps), but not with blood group Lea (Galbeta1-->3[Fucalpha1-->4]GlcNAc) substances, suggesting that residues and optimal density of alpha1-2 linked LFuc to Gal at the non-reducing end of glycoprotein ligands are essential for lectin-carbohydrate interactions. Blood group precursors, Galbeta1-3GalNAc (T), GalNAcalpha1-Ser/Thr (Tn) containing glycoproteins and N-linked plasma gps, gave only negligible affinity. Among the mammalian glycotopes tested, Ah, Bh and H determinants were the best, being about 5 to 6.7 times more active than LFuc, but were weaker than p-nitrophenylalphaFuc indicating that hydrophobic environment surrounding the LFuc moiety enhance the reactivity. The hierarchy of potency of oligo- and monosaccharides can be ranked as follows: p-nitrophenyl-alphaFuc > Ah, Bh and H > LFuc > LFucalpha1-->2Galbeta1-->4Glc (2'-FL) and Galbeta1-->4[LFucalpha1-->3]Glc (3'-FL), while LNDFH I (Leb hexa-), Lea, Lex (Galbeta1-->4[Fucalpha1-->3]GlcNAc), and LDFT (gluco-analogue of Ley) were inactive. From the present observations, it can be concluded that the combining site of AAA should be a small cavity-type capable of recognizing mainly H/crypto H and of binding to specific polyvalent ABH and Leb glycotopes.     

Mediation of serotonin-induced hyperventilation via 5-HT3-receptor in European eel Anguilla anguilla

The effects of serotonin (5-hydroxytryptamine) on ventilation were investigated by continuous measurements of intrabuccal pressure in unrestrained eel. Intravenous administration of 5-hydroxytryptamine (30 g·kg^-1) caused a large increase in ventilatory frequency (+100%) and amplitude (+140%). The 5-hydroxytryptamine-induced hyperventilation was blocked by the 5-HT₃-receptor antagonists metoclopramide (1.0 mg·kg^-1) or MDL72222 (1.0 mg·kg^-1), and was insensitive to the 5-HT_1/2-receptor antagonist methysergide (3.0 mg·kg^-1) and to the 5-HT₄-receptor antagonist DAU 6285 CL (3.0 mg·kg^-1). The hyperventilatory response to 5-hydroxytryptamine could be mimicked by the 5-HT₃ receptor agonist 1-phenylbiguanide (300 g·kg^-1). These results strongly implicate the 5-HT₃-receptor as the mediator of the 5-hydroxytryptamine-induced hyperventilation in eel.Abbreviations a.u. arbitrary units - 5-HT 5-hydroxytryptamine - SEM standard error of mean - VA ventilatory amplitude - VF ventilatory frequency - RBI 1-phenylbiguanide     

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.     

Different effects of cGMP and cAMP in the intestine of the European eel,Anguilla anguilla

The regulation of salt absorption in the sea water cell intestine was studied by evaluating the effects of theophylline, 8 Br cyclic adenosine monophosphate, 8 Br cyclic guanosine monophosphate, atriopeptin III, porcine vasoactive intestinal peptide and prostaglandin E ₁ on the short-circuit current, the transepithelial voltage difference and conductance and on the dilution potentials. It was shown that theophylline increased the transepithelial conductance and reduced the magnitude of the dilution potentials, indicating that the drug increase the anion conductance of the tight junctions. In addition its inhibitory effect on short-circuit current and transepithelial voltage difference suggests that theophylline also affects the transcellular transport mechanisms. It was shown that 8 Br cyclic guanosine monophosphate and 8 Br cyclic adenosine monophosphate affect transcellular mechanisms underlying Cl^– transport since both compounds reduced short-circuit current and transepithelial voltage difference; however, cyclic adenosine monophosphate is less effective since unlike cyclic guanosine monophosphate, even at maximal concentration, it was not able to completely abolish transepithelial voltage difference and short-circuit current. The effects of cyclic guanosine monophosphate and cyclic adenosine monophosphate were not additive even if cyclic guanosine monophosphate may produce further inhibition of ion transport in 8 Br cyclic adenosine monophosphate-treated tissues. In addition, cyclic guanosine monophosphate but not cyclic adenosine monophosphate reduced the magnitude of the dilution potentials, suggesting that cyclic guanosine monophosphate acts also on the paracellular pathway. Rat atriopeptin III, a peptide known to increase cyclic guanosine monophosphate cellular levels, behaved like 8 Br cyclic guanosine monophosphate since it lowered the dilution potentials and reduced short-circuit current and transepithelial voltage difference to near zero values, suggesting that the hormone modulates both paracellular and transcellular transport mechanisms, probably acting on the Na-K-2Cl cotransport. Agents acting via cyclic adenosine monophosphate, like porcine vasoactive intenstinal peptide and prostaglandin, behaved like 8 Br cyclic adenosine monophosphate. They were less effective in inhibiting ion transport and did not interfere with the paracellular pathway.Abbreviations AP III rat artriopeptin III - 8 Br cAMP 8 Br cyclic adenosine monophosphate - 8 Br cGMP 8 Br cyclic guanosine monophosphate - g _t transepithelial conductance - I _sc short circuit current - IC ₅₀ half-maximal inhibitory concentration - NaK ATPase Na-K-adenosine monophosphate - NPPB 5-nitro-2-(3-phenylpropylamino)-benzoic acid - PGE prostaglandin E ₁ - R _t tissue resistance - SITS 4-acetamide-4-isothiocyano-stilbene-2,2-disulfonic acid - V _t transepithelial voltage difference - VIP porcine vasoactive intestinal peptide     

Structural studies of nerve terminals containing melanin-concentrating hormone in the eel,Anguilla anguilla

Summary Eels were adapted to black- or white-coloured backgrounds and the pituitary glands were prepared for light and electron microscopy. Immunocytochemical staining was used to study the distribution of the neurohypophysial melanin-concentrating hormone in the neurointermediate lobe. The hormone was located in small, elliptical, electron-opaque neurosecretory granules, measuring approximately 120×90 nm. The neurones terminated on blood vessels in the centre of the neurohypophysis and on the basement membrane separating neural and intermediate lobe tissues. The results of both light and electron immunocytochemistry and of radioimmunoassay are consistent with a higher rate of hormone release from eels adapted to white backgrounds than from those adapted to black backgrounds. In addition to this, when fish that had been adapted to white tanks were transferred to black tanks, there was an accumulation of irMCH in the gland and an increased numerical density of secretory granules at nerve terminals. These results reinforce the proposal that MCH is released during adaptation to a white background, to cause melanin concentration and to inhibit MSH release, and that its release is halted in black-adapted fish.     

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 morphometric analysis of regional differences in myotomal muscle ultrastructure in the juvenile eel (Anguilla anguilla L.)

Summary Subpopulations of fast and slow fibres within the trunk musculature of elvers were examined using morphometric analysis of electron micrographs. Fibre regions were characterised by their histochemical staining characteristics, and individual fibres located using a coordinate mapping system utilising morphological features as reference points. Percentages of fibre volume occupied by mitochondria, myofibrils, sarcoplasmic reticulum (S.R.), and T-system were determined in each of the fibre groups, along a transect from the skin to the vertebral column (fibres 1–14, respectively).The fine structure of slow (red) fibres (1–2 fibres deep) is relatively homogeneous throughout its range, giving mean values for mitochondria, 21.4%; myofibrils, 61.0%; S.R., 2.10%; T-system, 0.31%. The fibres are relatively small (204 m²) and the mitochondrial cristae poorly developed.In contrast, there is a marked heterogeneity in the ultrastructure of fast (white) fibres, dependent on both position and size. The moderately small (333 m²) superficial fast fibres (3–4 fibres deep) have a significantly higher mitochondrial content (7.6%) than the larger deep fibres (1.2%) (6–12 fibres deep, 775 m²). The mean fractional volumes occupied by myofibrils, S.R., and T-system in the deep fibres are: 80.4%, 5.95%, and 0.38%, respectively. Fibres < 100 m² constitute up to 5% of the fast muscle and have a significantly higher mitochondrial volume (4.3%), more glycogen granules, and a slightly lower volume of S.R. (5.57%) than larger fibres.It is suggested that metabolic subpopulations of fast fibres correspond to different stages of fibre growth. The relatively poorly developed S.R. of eel fast muscle is thought to be correlated with the low frequency, high amplitude nature of the propagated waveform found in anguilliform locomotion.     

Catecholamine fluorescence in the pituitary of the eel,Anguilla anguilla,with special reference to its variation during background adaptation

Summary In the neuro-intermediate lobe (NIL) of the eel, Anguilla anguilla, a specific formaldehyde-induced fluorescence, indicating a catecholamine (CA) innervation, has been demonstrated in the neural lobe processes. Microspectrofluorimetric analyses and pharmacological treatments indicate noradrenaline or dopamine or both to be responsible for the fluorescence.The fluorescence in the NIL has displayed a definite tendency toward variation during the adaptation to a white and to a black background. The highest amounts of fluorescence were generally found in animals adapted to a black background, especially when adapted for a rather long period, and in animals recently transferred to a white background. The lowest amounts of fluorescence were generally found in animals adapted to a white background.This and the result of injections of CA-depleting drugs suggest that the monoaminergic nerves are active when the animal is on a white background, inhibiting the MSH release directly or indirectly or both, or in co-operation with other factors.Specific green fluorescent structures were also found in other parts of the neural lobe supplying the pars distalis.In some pharmacologically untreated specimens and in animals treated with CA-depleting drugs, the intermedia cells fluoresced. Microspectrofluorimetric analyses indicated that this fluorophore was not a CA.We wish to express our sincere thanks to Miss Ingrid Carlsen for excellent technical assistance, Mr. Lajos Erdös for the photography and the technical staff of the Department of Histology in Lund. We are also indepted to Dr. Anders Björklund for valuable discussion and advice.Supported by grants from the Swedish Natural Science Research Council, the University of Lund, and the Royal Physiographic Society of Lund.     

Effects of eel (Anguilla anguilla L.) removals from selected sites of a stream on its subsequent densities

We assessed the effect of eel (Anguilla anguilla) removal from three sites of a Cantabrian stream upon its subsequent densities. In the first sample (Sept. 1986) numbers and densities were estimated as 43, 45 and 84 ind and 3490, 3030 and 3750 ind ha ⁻¹. Removal of these eels reduced the subsequent numbers and densities which, except on two occasions, were never reached again during the two years (eleven estimates) of study. Highest densities were recorded in the uppermost site in May and July, 1987, coincident with a strong drought and the lowest densities occurred in 1988 during a normal wet year. We hypothesize first that, because of a selective underground homing behaviour of eels, electro-fishing is inefficient and results in underestimates of the population. Second, seasonal variations of water discharge and droughts may not influence the homing behaviour of'eels until a threshold of dryness is reached. If this occurs, eels abandon their refuges and move towards the stream bottom. It seems that in Arroyo Chabatchos this threshold was exceeded in the summer of 1987 when the highest densities were estimated. The re-colonization of these sites experimentally depleted of eels, is a slow procces that lasts for, at least, two years.     

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.     

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.     

The cardiac effects of neurohypophysial hormones in the eel,Anguilla japonica (Temminck and Schlegel)

Summary The cardiac effects of neurohypophysial hormones in the Japanese eel, Anguilla japonica (Temminck and Schlegel), were studied in isolated atrial preparations at room temperatures of 17–20°C, 25–28°C, or 28°C. Arginine vasotocin (AVT), oxytocin (OXY), mesotocin (MSN), and isotocin (ISN) produced dose-related positive chronotropic and inotropic responses. Arginine vasopressin (AVP) was not effective. The effects of ISN on the atrial rate and tension were not affected in the presence of phentolamine or propranolol, which are and adrenergic antagonists, respectively. The activity of the eel heart and the effects of neurohypophysial hormones are temperature-dependent. The functional significance of these cardiac effects of neurohypophysial hormones is not known.     

Purification and characterization of dermatan sulfate from the skin of the eel,Anguilla japonica

Glycosaminoglycans were isolated from the eel skin (Anguilla japonica) by actinase and endonuclease digestions, followed by a beta-elimination reaction and DEAE-Sephacel chromatography. Dermatan sulfate was the major glycosaminoglycan in the eel skin with 88% of the total uronic acid. The content of the IdoA2Salpha1-->4GalNAc4S sequence in eel skin, which shows anticoagulant activity through binding to heparin cofactor II, was two times higher than that of dermatan sulfate from porcine skin. The anti-IIa activity of eel skin dermatan sulfate was determined to be 2.4 units/mg, whereas dermatan sulfate from porcine skin shows 23.2 units/mg. The average molecular weight of dermatan sulfate was determined by gel chromatography on a TSKgel G3000SWXL column as 14 kDa. Based on 1H NMR spectroscopy, the presence of 3-sulfated and/or 2,3-sulfated IdoA residues was suggested. The reason why highly sulfated dermatan sulfate does not show anticoagulant activity is discussed. In addition to dermatan sulfate, the eel skin contained a small amount of keratan sulfate, which was identified by keratanase treatment.     

Long-term effects of hydropower installations and associated river regulation on River Shannon eel populations: mitigation and management

The Shannon, Ireland’s largest river, is used for hydroelectricity generation since 1929. Subsequently, the Electricity Supply Board assumed responsibility for management of its eel stocks, due to the impact of the hydro-dam on recruitment to the commercial fishery. In order to negate a decline in juvenile recruitment resulting from the installation of hydroelectric facilities, management was focused on stocking lakes with elvers and fingerling eels. These were trapped at the hydropower facilities and in estuarine tributaries during their up-stream migrations. Due to the decline of natural recruitment in more recent times, attempts have also been made to develop an estuarine glass eel fishery. Stock levels are then monitored through annual surveys of the population trends of juvenile (glass eel, elver), growing phase (yellow eel) and downstream migrating pre-spawners (silver eels). Survey results and fishery management programmes are reviewed in this article. In addition to the long-term effects the hydroelectric facilities have had on the stock levels, there is also an annual effect on the migratory patterns of downstream migratory silver eels. In the lower reaches of the river system flow rates are regulated by the hydroelectric stations. We review previous work that had highlighted the importance of flow in determining the timing of the silver eels migrations, and assess the relationship between flow and migration in more detail through the use of hydroacoustic and telemetric studies. Current research on seaward migrating silver eel populations, suggests that spawner escapement rates can most effectively be increased by trapping migrating eels at fishing weirs located up-stream of the power station and transporting them towards the estuary. Guest editors: R. L. Welcomme & G. Marmulla Hydropower, Flood Control and Water Abstraction: Implications for Fish and Fisheries