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.     

Salinity-linked growth in anguillid eels and the paradox of temperate-zone catadromy

Temperate-zone anguillid eels use both saline (marine or brackish) and fresh waters during their continental phase, but use of fresh waters is paradoxical because on average these fishes grow more rapidly in saline than in fresh waters. Based on data from anguillid eels whose habitat-residency histories had been determined by Sr:Ca otolithometry, superiority of growth rates in saline water is much greater in American eels Anguilla rostrata in north-eastern North America (mean saline:fresh growth rate ratio 2·07) than in European Anguilla anguilla , Japanese Anguilla japonica and shortfinned Anguilla australis eels (range of mean ratios 1·12–1·14). Data from A. rostrata in the Hudson Estuary, U.S.A., and Prince Edward Island, Canada, were used to test adaptive explanations of catadromous migrations. The hypothesis that lower mortality in fresh water offsets faster growth in saline water was not supported because loss (mortality + emigration ) rates did not vary between saline and fresh zones of the Hudson Estuary. Hypotheses that anguillid eels move to fresh water to escape from larger anguillid eels in saline water or to evaluate habitat quality were not supported by size and age distributions. Catadromy in temperate-zone anguillid eels increases the diversity of occupied habitats and therefore lowers fitness variance caused by environmental fluctuations. Catadromy in temperate-zone anguillid eels could be due to natural selection for maximum geometric mean fitness which is sensitive to fitness variance. Temperate-zone catadromy might also be maladaptive, at least in local areas, due to shifts over time in selective pressures or to inability of panmictic genetic systems to adapt to local conditions.     

Anguilla rostrata glass eel migration and recruitment in the estuary and Gulf of St Lawrence

This study describes catches of Anguilla rostrata glass eels and associated oceanographic conditions in the St Lawrence Estuary and Gulf. Ichthyoplankton survey data suggest that they enter the Gulf primarily in May, migrate at the surface at night, and disperse broadly once they have passed Cabot Strait. They arrive in estuaries beginning at about mid-June and through the month of July. Migration extends west up to Québec City, in the freshwater zone of the St Lawrence Estuary, 1000 km west of Cabot Strait. Anguilla rostrata glass eels travel between Cabot Strait and receiving estuaries at a straight-line ground speed of c. 10–15 km day⁻¹. Catches of fish per unit effort in estuaries in the St Lawrence system are much lower than those reported for the Atlantic coast of Canada. Low abundance of A. rostrata glass eels in the St Lawrence system may be due to cold surface temperatures during the migration period which decrease swimming capacity, long distances from the spawning ground to Cabot Strait and from Cabot Strait to the destination waters (especially the St Lawrence River), complex circulation patterns, and hypoxic conditions in bottom waters of the Laurentian Channel and the St Lawrence Estuary.     

Validation of daily otolith increments in glass-phase American eels Anguilla rostrata (Lesueur) during estuarine residency

Prior to making inferences from otoliths about the residence time and growth rate of glass-phase anguillid eels Anguilla in estuaries, it is necessary to validate the deposition rate of microincrements in the otoliths. Glass-phase American eels Anguilla rostrata (Lesueur), which had been captured near the mouth of an estuary in Maine, USA, prior to freshwater exposure, deposited increments at a daily rate at ambient temperature and salinity in a field and laboratory study. The regression for glass eels not possessing a transition ring was: I=0.976(D-1)+0.434, where I is the number of otolith increments distal to a fluorescent mark placed on the otolith at the beginning of the experiment, and D is the number of days in the experiment, which ranged from 7 to 49. The slope was not significantly different than 1. Unexpectedly, many glass eels deposited the transition ring during the experiment, although this ring had previously been thought to mark entry into fresh water. The regression for these glass eels was: I=0.961(D-1)-3.880, and the slope was not significantly different than 1. The negative intercept suggests that approximately 4 days were lost from the otolith record during deposition of the ring. This study demonstrated daily deposition of increments prior to freshwater exposure and demonstrated that deposition of the transition ring is not linked to freshwater entry.     

Stable isotope analyses provide new insights into ecological plasticity in a mixohaline population of European eel

Recent studies have shown that anguillid eel populations in habitats spanning the marine–freshwater ecotone can display extreme plasticity in the range of catadromy expressed by individual fishes. Carbon and nitrogen stable isotope analysis was used to differentiate between European eels (Anguilla anguilla) collected along a short (2 km) salinity gradient ranging from <1‰ to ~30‰ in Lough Ahalia, a tidal Atlantic lake system. Significant differences were recorded in mean δ¹³C, δ¹⁵N and C:N values from eels collected from fresh, brackish and marine-dominated basins. A discriminant analysis using these predictor variables correctly classified ca. 85% of eels to salinity zone, allowing eels to be classified as freshwater (FW), brackish (BW) or marine (MW) residents. The results of the discriminant analysis also suggested that a significant proportion of eels moved between habitats (especially between FW and BW). Comparisons of several key population parameters showed significant variation between eels resident in different salinity zones. Mean condition and estimated age was significantly lower in MW eels, whilst observed length at age (a correlate of growth) was significantly higher in MW eels, intermediate in BW and lowest in FW eels. This study has demonstrated that the ecology of eels found along a short salinity gradient can be extremely plastic and that stable isotope analysis has considerable utility in demonstrating intra-population variation in diadromous fishes.     

Migratory patterns and contribution of stocking to the population of European eel in Lithuanian waters as indicated by otolith Sr:Ca ratios

Otolith Sr:Ca ratios were examined to evaluate the contribution of the stocked eel Anguilla anguilla elvers, which have been stocked in Lithuanian waters and mixed with naturally recruited eels for several decades, to the native eel population. Stocked eels were identified by the freshwater signature (Sr:Ca ratios <2·24 × 10⁻³) on the otolith after the glass eel stage. Naturally recruited eels, that had migrated through the North and Baltic Seas, were characterized by an extended seawater and brackish-water signature (Sr:Ca ratios >3·23 × 10⁻³) after the glass eel stage. Of 108 eels analysed, 21 eels had otolith Sr:Ca ratio profiles consistent with stocking while 87 showed patterns of natural recruitment. The ages of naturally recruited eels arriving in Lithuanian fresh waters varied from 1 to 10 years, with a mean ±  s.d . age of 5·2 ± 2·1 years. Eels from the inland Lake Baluošai were all freshwater residents of stocked origin. Stocked eels, however, accounted for only 20% of the eels from the Curonian Lagoon and 2% of eels sampled in Baltic coastal waters. This finding does not support the hypothesis that the eel fishery in the Curonian Lagoon depends mostly on stocking.     

Variability in growth of longfinned eels among coastal catchments of south‐eastern Australia

Longfinned eels Anguilla reinhardtii were captured by both fishery‐dependent and independent sampling methods from three rivers in New South Wales, south‐eastern Australia. Growth rates were examined in two zones (fresh water and tidal) in the Hacking, Hawkesbury and Clarence Rivers. Mean annual growth increments of sampled longfinned eels ranged from 30 to 60 mm year⁻¹ using age‐length analyses and up to 167 mm year⁻¹ based on tag‐recapture model estimates (GROTAG), with both methods showing high intra‐ and inter‐population variability. Growth was significantly faster in younger (5–15 years) fish than older (>15 years) fish, with females growing an average 10 mm year⁻¹ faster than males of similar age and capture location. Longfinned eels found in tidal areas grew significantly faster than those in non‐tidal freshwater areas as a result of longer growing seasons in the highly productive estuarine habitats. Other possible factors influencing variability in growth rates for this species include habitat preference, density and fishing pressure.     

Ecological aspects of the Japanese eel, Anguilla japonica, collected from coastal areas of Japan

The ecological characteristics of 597 yellow and silver-stage Japanese eels, Anguilla japonica, were examined and compared among collection sites located at three different latitudes of Japan (Amakusa Islands, Mikawa Bay, and Sanriku Coast) to provide basic data on this unusual catadromous fish species. Eels were sexed and their total length, body weight, age, and growth rate based on otolith analysis was compared among sexes, stages, and collection sites. The overall sex ratio favored females (94%), but the sex ratio differed among the three locations. The frequency of females was highest in the coastal waters at Sanriku in the north (100%), next highest at Mikawa Bay in central Japan (95%), and lowest in the Amakusa Islands in the south (70%). Silver eel males ranged from 41.2-66.3 cm in length and 4-10 years in age, and silver eel females from 44.3-97.2 cm in length and 5-17 years in age. Female eels generally grew faster (8.7+/-2.2 cm/year) than males (6.4+/-2.6 cm/year), and the growth rate slowed in the older eels. The growth rate of A. japonica at all three sites was much faster than that of other temperate anguillid species (< 4 cm/year), and their age at maturation was younger than that of other temperate species (approximately 7 to > 50 years), suggesting this species has important ecological differences from other similar species.     

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, pigmentation and activity of juvenile Japanese eels in relation to temperature and fish size

The growth and activity of juvenile Japanese eels Anguilla japonica in different pigmentation stages from the glass eel to the elver stage were studied in the laboratory at 15, 20 and 25° C. The growth and activity of the eels were significantly influenced by both temperature and fish size. Growth rate generally declined with increasing fish size, and fish were least active and experienced a low growth during the pigmenting stage at all temperatures. They were nocturnal and spent significantly more time moving (swimming, feeding and moving over the substratum) at 20 and 25° C than at 15° C at night within each pigmentation stage. Accordingly, they grew significantly faster at 20 and 25° C than at 15° C throughout the study. The development of pigmentation appeared to be dependant on water temperature but not on fish size. This study suggested that the growth and activity of juvenile Japanese eels were positively correlated, because fish were least active and grew slowest at low temperature (15° C) or during the pigmenting stage at all temperatures.     

Diverse migration strategy between freshwater and seawater habitats in the freshwater eel genus Anguilla

The freshwater eels of the genus Anguilla, which are catadromous, migrate between freshwater growth habitats and offshore spawning areas. A number of recent studies, however, found examples of the temperate species Anguilla anguilla, Anguilla rostrata, Anguilla japonica, Anguilla australis and Anguilla dieffenbachii that have never migrated into fresh water, spending their entire life history in the ocean. Furthermore, those studies found an intermediate type between marine and freshwater residents, which appear to frequently move between different environments during their growth phase. The discovery of marine and brackish-water residents Anguilla spp. suggests that they do not all have to be catadromous, and it calls into question the generalized classification of diadromous fishes. There has been little available information, however, concerning migration in tropical Anguilla spp. Anguilla marmorata, shows three fluctuation patterns: (1) continuous residence in fresh water, (2) continuous residence in brackish water and (3) residence in fresh water after recruitment, while returning to brackish water. Such migratory patterns were found in other tropical species, Anguilla bicolor bicolor and Anguilla bicolor pacifica. In A. b. bicolor collected in a coastal lagoon of Indonesia, two further patterns of habitat use were found: (1) constantly living in either brackish water or sea water with no freshwater life and (2) habitat shift from fresh water to brackish water or sea water. The wide range of environmental habitat use indicates that migratory behaviour of tropical Anguilla spp. is facultative among fresh, brackish and marine waters during their growth phases after recruitment to the coastal areas. Further, the migratory behaviours of tropical Anguilla spp. appear to differ in each habitat in response to inter and intra-specific competition. The results suggest that tropical Anguilla spp. have a flexible pattern of migration, with an ability to adapt to various habitats and salinities. The ability of anguillids to reside in environments of various salinities would be a common feature between tropical and temperate species without a latitudinal cline. Thus, the migration of Anguilla spp. into fresh water is clearly not an obligatory behaviour. This evidence of geographical variability among Anguilla spp. suggests that habitat use is determined by environmental conditions in each site.     

The induction of maturation and ovulation in American eels, Anguilla rostrata (LeSueur), and the relevance of chemical and visual cues to male spawning behaviour

Female American eels, Anguilla rostrata (LeSueur), were artificially matured with injections of salmon and carp pituitary and human chorionic gonadotropin. In vivo ovulation was induced with 4-pregnene-17α,20β-diol-3-one and eggs were spontaneously released. Eggs were fertilized in vitro and survived to the gastrula stage. Males were matured with injections of human chorionic gonadotropin. They were attracted by the sight and odour of maturing and mature females. Ovulated females released a sex pheromone which was especially attractive to mature males and triggered the release of sperm.     

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.     

Natural hybrids in Atlantic eels (Anguilla anguilla, A. rostrata): evidence for successful reproduction and fluctuating abundance in space and time

The outcome of natural hybridization is highly variable and depends on the nonexclusive effects of both pre- and post-mating reproductive barriers. The objective of this study was to address three specific questions regarding the dynamics of hybridization between the American and European eels (Anguilla rostrata and Anguilla anguilla). Using 373 AFLP loci, 1127 eels were genotyped, representing different life stages from both continents, as well as multiple Icelandic locations. We first evaluated the extent of hybridization and tested for the occurrence of hybrids beyond the first generation. Second, we tested whether hybrids were randomly distributed across continents and among Icelandic sampling sites. Third, we tested for a difference in the proportion of hybrids between glass eel and yellow eel stages in Iceland. Our results provided evidence for (i) an overall hybrid proportion of 15.5% in Iceland, with values ranging from 6.7% to 100% depending on life stages and locations; (ii) the existence of hybrids beyond the first generation; (iii) a nonrandom geographic distribution of hybrids in the North Atlantic; and (iv) a higher proportion of first and later generation hybrids in yellow eels compared to glass eels, as well as a significant latitudinal gradient in the proportion of hybrids in Icelandic freshwater. We propose that the combined effect of both differential survival of hybrids and variation in hybridization rate through time best explain these patterns. We discuss the possibility that climate change, which is impacting many environmental features in the North Atlantic, may have a determinant effect on the outcome of natural hybridization in Atlantic eels.     

Determination of the age of young American eels, Anguilla rostrata, in fresh water, based on otolith surface area and microstructure

The time elvers of the American eel, Anguilla rostrata , spend in an estuary prior to their migration into fresh water was assessed. A distinct mark was formed on elvers' otoliths during their first 2 to 3 weeks in the river estuary. This mark was used to distinguish between growth in fresh water and in salt water. Migrating eels collected at a falls 4 km from the estuary exhibited bimodal length and weight distributions. Frequency distributions showed that eels collected in the estuary were smaller and had smaller otoliths than eels collected at the falls, indicating that elvers do not reach the falls in the same year as they enter the estuary. The three modal groups most probably represent three age–classes. However, the otoliths of elvers collected in the estuary had only the mark of transition whereas eels in the first and second mode at the falls usually had two rings (1–4) and four rings (3–6) per otolith, respectively, in addition to the mark of transition, as viewed under SEM. The possibility that ring formation is not annual means that the use of otoliths for the age determination of eels in this study has not been validated.     

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.     

Sex Determination in Freshwater Eels and Management Options for Manipulation of Sex

Catadromous eels enter fresh water as sexually undifferentiated glass eels and develop into males and females before migrating back to sea as silver eels. Females develop ovaries directly from the ambiguous primordial gonad whereas males pass through a transitional intersexual stage before developing testes. Eels have sex-specific life-history strategies. Males may grow faster than females initially, but this difference is soon reversed and females attain a greater age- and size-at-metamorphosis than males. Male fitness is maximized by maturing at the smallest size that allows a successful spawning migration (a time-minimizing strategy) whereas females adopt a more flexible size-maximizing strategy that trades off pre-reproductive mortality against fecundity. Although heteromorphic sex chromosomes have been identified in some species, the sex of developing gonads is labile and gender is determined principally by environmental factors. Individuals experiencing rapid growth prior to gonad differentiation tend to develop as males, whereas eels that grow slowly initially are more likely to develop as females. Paradoxically, males tend to predominate under conditions of high density, which may be because a male “grow quickly, mature early” strategy increases an individual’s chances of survival during periods of intraspecific competition. High temperatures and saline conditions have also been proposed to favor development as males but experimental studies have failed to demonstrate a clear effect of either on sex determination. High proportions of female silver eels migrating from some upstream areas, lakes and large rivers may be due to low population density or poor conditions for growth in these habitats. Manipulating sex ratios in favor of females has the potential to increase eel production in aquaculture and to buffer natural populations against fishing pressure. Sex steroids (oestrogens and phytoestrogens) have a strong feminizing effect on undifferentiated individuals and are most effective when targeted at younger eels and administered at high doses for prolonged periods. Modifying local environmental conditions, in particular reducing eel density and limiting interference and social stress, may also promote the development of females. Further research into the timing and mechanisms of sex determination in eels is required to effectively and efficiently manipulate sex for conservation and/or economic benefit.     

Age and growth of yellow eels, Anguilla anguilla, in the estuary of the Guadalquivir river (south-west Spain)

A total of 1068 eels were examined from a population located in the Guadalquivir river estuary (37°N, 6°25'W). Maximum ages recorded were 4 + (males) and 7+ (females), and maximum lengths were 39-1 cm (males) and 54.1 cm (females). No growth was recorded between November and April, most occurring in May and, to a lesser extent, in June-October. Females grew to be larger than males. A classification analysis, based on 17 different European eel populations revealed that populations in brackish waters grew faster than those in fresh waters, but latitude also had an influence. Length-weight relationships obtained for three eel categories (males, females and undifferentiated) were used to estimate relative condition: condition cycles were similar between sexes, with increases in autumn and decreases in winter. There were monthly fluctuations in the sex ratio, and females dominated significantly in the combined catch (234 males/276 females).     

Recent visitations by eels to Sable Island, Canada, confirmed by parasites

The presence of immature stages of Proteocephalus macrocephalus in nine-spined stickleback Pungitius pungitius , four-spined stickleback Apeltes quadracus , three-spined stickleback Gasterosteus aculeatus , and mummichog Fundulus heteroclitus from Sable Island ponds was confirmed using scolex morphology. The occurrence of this eel-specific parasite in these accidental hosts provides evidence for recent visits by eels Anguilla rostrata to the isolated island in the North-west Atlantic Ocean off the east coast of Canada.     

The swimbladder nematode Anguillicola crassus in American eels (Anguilla rostrata) from middle and upper regions of Chesapeake Bay.

The patterns of infection of American eels Anguilla rostrata, with the introduced swimbladder nematode Anguillicola crassus, in tributaries of middle and upper Chesapeake Bay are described. A total of 423 subadult eels was collected from 8 Bay tributaries from spring 1998 to fall 1999. Also, 30 elvers were collected from Ocean City, Maryland, in spring 1998. The numbers of juvenile and adult specimens of A. crassus in the swimbladder wall and lumen were counted. No elvers were infected. In subadult eels, prevalence of adult and juvenile stages combined ranged from 13% to 82%; mean intensity ranged from 2.6 to 9.0 worms per eel. Infection levels were highest for Susquehanna River eels (northernmost river) and lowest in the southernmost sites: St. Jerome's Creek and the Pocomoke River. Although eels from these 2 localities were larger, the low infection rates there are most likely due to reduced transmission in higher salinity water and not to eel size. Eels with both adult and juvenile stages of A. crassus were more common than expected by chance. This might be explained by inhibition of juveniles migrating into the swimbladder lumen when adults are already present there.