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.     

Experimental analysis of the thermal and salinity preferences of glass-eels, Anguilla anguilla (L.), before and during the upstream migration

During their upstream migration European glass-eels, Anguilla anguilla (L.), encounter a series of varying environmental situations. The migration requires a sequence of physiological adaptations determined by the different chemico-physical conditions they meet. Temperature and salinity are two of the most important factors. It is reasonable that glass-eels may utilize them as cues to orientation. Laboratory experiments were designed to elucidate the thermal and salinity preferences of glass-eels. These were assessed by examining the choices of specimens caught either at sea and then kept in salt water (33%), or in the Arno river and then reared in fresh water. Water flows, triggering the rheotactic reaction, prompted glass-eels to choose between two different salinities and/or temperatures. The results confirm the preference of glass-eels for flows whose temperature does not differ from that of acclimation. Specimens tested towards two water flows, both at different temperatures from that of acclimation, preferred the colder. Fresh water was usually preferred to salt water, this preference being not so marked in the case of the glass-eels caught at sea and thus not yet adapted to fresh water. Clear-cut choices were recorded when one of the tested flows presented both the preferred temperature and preferred salinity. When only one of the two parameters reproduced the preferred situation, the choices were differently affected by temperature and salinity at different values of temperature. When the temperature of both flows was below 11–12°C, glass-eels preferred fresh water; at higher temperatures the colder of the two flows was preferred, even if salty.     

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.     

Effect of change of habitat (sea and fresh water) on in vivo thyroglobulin synthesis in Atlantic glassed eels (Anguilla anguilla L.)

Thyroid biosynthesis in glassed eels (Anguilla anguilla L.) was studied to establish whether salinity changes could affect it, when they live in sea water or in fresh water containing 125I. Aqueous extrait of homogenized cephalic heads of glassed eels contains an iodinated protein 17-19 S having thyroglobulin-like properties and including iodotyrosins (MIT and DIT) and thyroid hormones (3 and T4). Biosynthesis of this proteins is roughly twice more important in fresh water than in sea water at 19-21 degrees C and its specific radioactivity (125I) is practically double in fresh water.     

Salinitätspräferenzen bei Glasaalen und jungen Gelbaalen(Anguilla anguilla)

Preference experiments have been carried out on elvers and young eels in order to assess locomotory responses to different salinity conditions. Employing different test apparatus it was established that elvers preferred fresh water to water of 18 ‰ and 36 ‰ S. There was no significant difference between responses to water of 18 ‰ and 36 ‰ S. When young yellow eels were offered different salinities (fresh water, 18 ‰ and 36 ‰ S) in tubes, a preference for water of 18 ‰ S was noted. This preference was not influenced by the different salinities in which the eels had previously been kept.     

Effect of salinity on hatching, survival and infectivity of Anguillicola crassus (Nematoda: Dracunculoidea) larvae

The effect of salinity on hatching, larval survival and infectivity of Anguillicola crassus was studied under experimental conditions using eggs obtained from naturally infected eels. Egg hatching rate, second-stage larval survival and larval infectivity were maximal in fresh water and declined with increase in salinity. Larvae survived up to 100 d in fresh water, 70 d in 50 % sea water and 40 d in 100% sea water. Infectivity experiments demonstrated that salinity influenced transmission success throughout the life cycle by decreasing total infectivity of the larval population in utero within female A. crassus and when larvae were free-living in the aquatic environment. Infectivity was age-dependent in relation to salinity. Larvae were infective to intermediate and paratenic hosts for up to 80 d in fresh water, 21 d in 50% sea water and up to 8 d in 100% sea water. The data confirm field observations that infection levels decrease with an increase in salinity. The study contributes to experimental verification of the colonization abilities of A. crassus and supports the hypothesis that A. crassus can be disseminated and transmitted in brackish water. The importance of regular monitoring and stringent hygiene practices in the transportation of eels is emphasized.     

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.     

Salinity,freshwater and agricultural water preferences of glass eels of the Japanese eel Anguilla japonica collected in southern Japan

Water-choice trial experiments revealed that Anguilla japonica glass eels collected in southern Japan possess strong preferences for fresh water and agricultural water. Their locomotor activity and preference for fresh water were higher and stronger, respectively, in this study when compared to previous studies conducted at lower temperatures. These results suggest that their locomotor activity and preference for fresh water is influenced by water temperature. The attraction to agricultural water indicates their upstream migration and habitat selection could be influenced by agricultural water.     

Variations in the migratory history of the tropical catadromous eels Anguilla bicolor bicolor and A. bicolor pacifica in south-east Asian waters

Fish movements between aquatic habitats of different salinity ranges (fresh, estuarine, marine) by the tropical catadromous eels Anguilla bicolor bicolor and A. bicolor pacifica were examined by analysing the otolith strontium and calcium concentrations of yellow (immature) and silver (mature) stage eels collected in south-east Asian (Indonesia, Malaysia and Vietnam) waters. The ratios suggest that all migratory-type eels, including freshwater, brackish water and marine residents, pass the river mouth. However, the habitat preference was different among the sites (countries). In Indonesia and Vietnam, most A. bicolor bicolor and A. bicolor pacifica were either marine or brackish water residents in this study. Alternatively, most A. bicolor bicolor were freshwater residents in Malaysia; such a typical catadromous migration pattern in these eels has not been found in previous studies. The wide range of otolith Sr:Ca in both subspecies indicates that the habitat use of these tropical eels was opportunistic among fresh, brackish and marine waters during their growth phases following recruitment to coastal areas. The geographical variability of migratory histories suggests that habitat use might be determined by the inter and intraspecific competition and environmental conditions at each site.     

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

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Evolutionary-physiological aspects of adaptation of the Pacific salmon fry of the Oncorhynchus genus to migration to the sea water

A complex of adaptive changes occurring in the Pacific salmon fry in the process of migration to the sea is described, including behavior, ion content in carcasses, and morphological changes in Stannius bodies, gill epithelium, and nephron tubular epithelium. Participating in experiments with transfer from fresh water into a two-layer aquarium (the lower layer - sea water, the upper layer - fresh water) were smolts of chum salmon and underyearlings of masu salmon as well as the trachurus and leiurus forms of the three-spined stickleback Casterosteus aculeatus. All fish, regardless of their salt preference, at once after placement into the two-layer aquarium, occupied the sea water zone, at the very bottom of the aquarium. After 1 h, there started brief excursions of masu salmon and chum salmon to the upper, fresh water layer; however, both forms of the three-spined stickleback did not participate in these excursions. After 12 h, the chum salmon settled down in the lower, sea water layer, while the masu salmon - in the upper, fresh water layer. Both forms of the three-spined stickleback never left the sea water layer and felt quite comfortably on the aquarium bottom. It seems that the high tolerance of the both stickleback forms to wide salinity limits allows them to choose the convenient position regardless of the water salt composition. By analyzing the material obtained for three years (2001-2003) on structure and functions of the gill epithelium chloride cells (CC), we have come to the conclusion that the fresh water fry of two salmon species, chum and masu salmons, caught at the same time and practically in the same water reservoirs can be divided into three groups. The underyearlings of the masu salmon as a rule are characterized by the thickened epithelium of secondary gill lamellae, but by a very small number of CC. In smolts of chum salmon, on the contrary, the epithelium is sufficiently thin, but enriched in the CC that demonstrate an active structure in the very beginning of migration to sea. However, with approaching the sea (and with an increase of terms of migration) the CC activity drops, but their amount does not change. And only after migration to the sea the CC activity rises again, although their amount seems to remain unchanged. The described peculiarities of behavior and of the ion composition regulation in the migrating salmon fry confirm the hypothesis that the salmons evolutionized in fresh water, that the Oncorhynchus genus appeared in large spaces of saltish waters, such as the Japan Sea at the period of the early Pleistocene, and that learning of fry of the Oncorhynchus genus (for instance, of O. gorbuscha and O. keta) is the most specialized in the salmons migrating to the sea, whereas the fresh water species of chars (Salvelinus) and of trouts (Salmo) are more primitive.     

Colonization, larval survival and epidemiology of the nematode Anguillicola crassus, parasitic in the eel, Anguilla anguilla, in Britain

In late 1987, immature Anguillicola crassus were reported for the first time in Britain from eels from two river systems. By late 1988, gravid adults were present in a number of rivers in the east of England in two discrete centres of distribution: one in East Anglia correlated with the route taken by lorries exporting eels to the continent, and one in the R. Thames correlated with the import of eels to London. The parasite was firmly established in the R. Trent, where prevalence levels reached 100% in some places. Laboratory investigations showed that adult parasites and their eggs remained viable even after infected eels had been maintained for 4 weeks in 100% sea water. Hatching of eggs declined with increasing salinity, but was not totally inhibited by sea water. Survival and infectivity of freeliving second stage larvae were maximal in natural fresh water (95% survival for 4 months, and 50% still infective to copepod intermediate hosts after 70 days), but declined in alkaline water and with increased salinity. Nevertheless, in 100% sea water, 50% of larvae were still infective after 8 days. Specificity to the intermediate host was low, and eels of all sizes could be infected. These characteristics, plus a high reproductive potential, give the parasite exceptional colonization potential and ability, enabling it to survive natural movements of eels from catchment to catchment and to increase rapidly within a new locality. The ability of free-living larvae to adhere to the substratum and survive in sea water enables them to survive in eel-transport lorries from which they will not readily be removed by flushing, the normal cleansing procedure. It is concluded that there were two separate introductions of the parasite to Britain; via the eel import trade through London, and, totally unexpectedly, via the eel export trade in lorries traversing East Anglia. The parasite is now firmly established in Britain and will continue to spread by natural movements of eels but especially by human-assisted movements of infected eels for stocking and market. This latter practice is recognized as a major factor in introducing and disseminating fish parasites.     

Evolutionary-physiological aspects of adaptation of the Pacific salmon fry of the oncorhynchus genus to migration to the sea water

A complex of adaptive changes occurring in the Pacific salmon fry in the process of migration to the sea is described, including behavior, ion content in carcasses, and morphological changes in Stannius bodies, gill epithelium, and nephron tubular epithelium. Participating in experiments with transfer from fresh water into a two-layer aquarium (the lower layer—sea water, the upper layer—fresh water) were smolts of chum salmon and underyearlings of cherry salmon as well as the trachurus and leiurus forms of the three-spined stickleback Casterosteus aculeatus. All fish, regardless of their salt preference, at once after placement into the two-layer aquarium, occupied the sea water zone, at the very bottom of the aquarium. After 1 h, there started brief excursions of cherry salmon and chum salmon to the upper, fresh water layer; however, both forms of the three-spined stickleback did not participate in these excursions. After 12 h, the chum salmon settled down in the lower, sea water layer, while the cherry salmon—in the upper, fresh water layer. Both forms of the three-spined stickleback never left the sea water layer and felt quite comfortably on the aquarium bottom. It seems that the high tolerance of the both stickleback forms to wide salinity limits allows them to choose the convenient position regardless of the water salt composition. By analyzing the material obtained for three years (2001–2003) on structure and functions of the gill epithelium chloride cells (CC), we have come to the conclusion that the fresh water fry of two salmon species, chum and cherry salmons, caught at the same time and practically in the same water reservoirs can be divided into three groups. The underyearlings of the cherry salmon as a rule are characterized by the thickened epithelium of secondary gill lamellae, but by a very small number of CC. In smolts of chum salmon, on the contrary, the epithelium is sufficiently thin, but enriched in the CC that demonstrate an active structure in the very beginning of migration to sea. However, with approaching the sea (and with an increase of terms of migration) the CC activity drops, but their amount does not change. And only after migration to the sea the CC activity rises again, although their amount seems to remain unchanged. The described peculiarities of behavior and of the ion composition regulation in the migrating salmon fry confirm the hypothesis that the salmons evolutionized in fresh water, that the Oncorhynchus genus appeared in large spaces of saltish waters, such as the Japan sea at the period of the early Pleistocene, and that learning of fry of the Oncorhynchus genus (for instance, of O. gorbuscha and O. keta) is the most specialized in the salmons migration to the sea, whereas the fresh water species of chars (Salvelinus) and of trouts (Salmo) are more primitive.     

Unravelling the life-history patterns and habitat preferences of the Japanese eel (Anguilla japonica) in the Pearl River,China

Eels have fascinated biologists for centuries due to their amazing long-distance migrations between freshwater habitats and very distant ocean spawning areas. The migratory life histories of the Japanese eel, Anguilla japonica, in the waters of south China are not very clear despite its ecological importance, and the need for fishery regulation and management. In this study, strontium (Sr) and calcium (Ca) microchemical profiles of the otoliths of silver eels were measured by X-ray electron probe microanalysis based on data collected from different habitats (including freshwater and brackish habitats), in the large subtropical Pearl River. The corresponding habitat preference characteristics were further analysed using redundancy analysis (RDA). A total of 195 Japanese eels were collected over 6 years. The collected individuals ranged from 180 to 771 mm in total length and from 8 to 612 g in body weight. Two-dimensional pictures of the Sr:Ca concentrations in otoliths revealed that the A. japonica in the Pearl River are almost entirely river eels, spending the majority of their lives in fresh water without exposure to salt water, while the catadromous migration time has delayed about 1 month in the Pearl River estuary in the past 20 years. RDA analysis further indicated that juveniles and adults preferred water with high salinity and high tide levels. Youth preferred habitats with high river fractals. Our findings contribute to a growing body of evidence showing that the eels are extremely scarce currently and conservation measures against them are imminent, including the protection of brackish and freshwater areas where they live in south China.     

How does salinity influence habitat selection and growth in juvenile American eels Anguilla rostrata?

The influence of salinity on habitat selection and growth in juvenile American eels Anguilla rostrata captured in four rivers across eastern Canada was assessed in controlled experiments in 2011 and 2012. Glass eels were first categorized according to their salinity preferences towards fresh (FW), salt (SW) or brackish water (BW) and the growth rate of each group of elvers was subsequently monitored in controlled FW and BW environments for 7 months. Most glass eels (78–89%) did not make a choice, i.e. they remained in BW. Salinity preferences were not influenced by body condition, although a possible role of pigmentation could not be ruled out. Glass eels that did make a choice displayed a similar preference for FW (60–75%) regardless of their geographic origin but glass eels from the St Lawrence Estuary displayed a significantly higher locomotor activity than those from other regions. Neither the salinity preferences showed by glass eels in the first experiment nor the rearing salinities appeared to have much influence on growth during the experiments. Elvers from Nova Scotia, however, reached a significantly higher mass than those from the St Lawrence Estuary thus supporting the hypothesis of genetically (or epigenetically) based differences for growth between A. rostrata from different origins. These results provide important ecological knowledge for the sustained exploitation and conservation of this threatened species.     

Densities and swimbladder development of juvenile American eels, Anguilla rostrata (Lesueur) as related to energetics of migration

Glass eels and elvers of the American eel were negatively buoyant. Those adapted to sea water were more dense (1.072 ± 0.001 g cm⁻³) than those adapted to fresh water (1.061 ± 0.001 g cm⁻³). Adaptation to fresh water increased relative body water content, but did not account for the observed decrease in total body density. Histological examination revealed the presence of a potentially functional swimbladder in the glass eels, although this hydrostatic organ did not becomegas-filled until after freshwater residency had occurred. Calculation of lift as used in the selective tidal transport mechanism suggests that hydrodynamic compensation for horizontal swimming during the estuarine phase of migration is energetically adaptive.     

Growth rate and age at migration of Anguilla anguilla

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

Dispersal of yellow phase Japanese eels <Emphasis Type="Italic">Anguilla japonica</Emphasis> after recruitment in the Kojima Bay-Asahi River system,Japan

The density, size and age distribution were investigated for 233 eels, Anguilla japonica, sampled in fresh and brackish water areas of the Kojima Bay-Asahi River system, Okayama, Japan, to evaluate the possible patterns of dispersal of eels that recruit to this area. Migratory histories of 183 eels were categorized into 5 types depending on the Sr and Ca concentrations in their otoliths: (1) brackish water residents (74 fish, 40.4%), which settled in saline water and remained until capture; (2) freshwater residents (46 fish, 25.1%), which settled in freshwater and remained until capture; (3) upstream shifters (3 fish, 1.6%), which settled in saline water and moved upstream into freshwater; (4) downstream shifters (53 fish, 29.0%), which settled in freshwater and moved downstream into saline water; (5) multiple habitat shifters (7 fish, 3.8%), which shifted their habitats between freshwater and saline water more than twice. For eels captured in the brackish water area, fish density decreased with distance in the downstream direction, while the size and age of eels increased. For eels captured in the freshwater area, size and age were greater than those in the upper-most brackish site. These observations suggest that eels in this system initially accumulate in the lower reaches of the river and then disperse in both upstream and downstream directions following their growth.     

Morphological Bases for Evolution of Functions

The morphological and morphometrical changes in the renal proximal tubular cells of the salmonOncorhynchus gorbuscha during spawning migration are described for the first time. The evaluation of the ultrastructural changes in the kidney of the adult humpback salmon allows concluding that the proximal tubular cells are affected by significant osmotic loads during spawning migration. Various destructive processes in the proximal tubular cells indicate a decrease of their functional activity in the fresh water. The analysis of the results of the study of the humpback salmon kidney ultrastructure during the anadromous migration allow suggesting that reduction of the amount of the most active cell organelles in the proximal tubule, such as mitochondria and the basolateral membrane system, is associated with a decrease of the number of ion pumps that operate less intensively in the fresh water. Such mechanism of the kidney functioning in the euryhaline fish appears to be formed in the course of evolution as an adaptation to the freshwater environment. The morphological and morphometrical changes in the proximal tubules of nephrons were described for the first time in Pacific salmon smoltsOncorhynchus keta, O. gorbuscha,O. Kisutch, andO. masou in environments with different salinity. The most marked response to the transfer to the sea water or to the calcium-enriched sea water was observed in the chum salmon smolts. In 48 h, the tubular diameter reached its peak, more than 72 μm, the tubular lumen also was very large, while the epithelium height was only slightly greater than that in the fresh water control. In spite of the considerable morphological changes, as soon as in 24 h (the Ca²⁺-enriched sea water) and in 48 h (the sea water) the ion content in smolt carcasses was within the physiological norm for the environment with enhanced salinity. These results indicate a high efficiency of the osmoregulatory system in smolts during their transfer from the fresh to the sea water.