Growth history and age at recruitment of European glass eels (Anguilla anguilla) as revealed by otolith microstructure

The growth history and age at recruitment of Anguilla anguilla Linnaeus, 1758 were studied, based on growth increments in sagittal otoliths of glass eels and elvers collected from the eastern Atlantic coast in 1989 and in 1990. The maximum otolith radius varied with pigmentation stage. Deposition of the transition ring was complete at Stage VIA₀. The size of the leptocephalus growth zone varied as a function of site, increasing from south to north. The oceanic migration of the leptocephali required less than one year.     

Relative contribution of migratory type on the reproduction of migrating silver eels, <Emphasis Type="Italic">Anguilla japonica</Emphasis>, collected off Shikoku Island,Japan

In order to understand the reproductive contribution among migratory types in the Japanese eel, Anguilla japonica, otolith strontium (Sr) and calcium (Ca) concentrations by X-ray electron microprobe analysis were examined for 37 silver eels collected in Kii Channel off Shikoku Island during the spawning migration season. The wide range of otolith Sr:Ca ratios indicated that the habitat use of A. japonica was not obligatory but facultative among fresh, brackish and marine waters during their growth phases after recruitment to the coastal areas as glass eels. Three migratory types, which were categorized as river eels, estuarine eels and sea eels were found. The estuarine eels were dominant (59%), followed by sea eels (22%) and river eels (19%). The low proportion of river eels from the spawning migration season suggested that the estuarine and sea eels inhabiting the nearby coastal areas might make a larger reproductive contribution to the next generation in this area.     

Early life history of the American conger eel (<Emphasis Type="Italic">Conger oceanicus</Emphasis>) as revealed by otolith microstructure and microchemistry of metamorphosing leptocephali

The early life history of the American conger eel, Conger oceanicus, was studied using otolith microstructure and chemical composition in metamorphosing leptocephali collected from New Jersey estuarine waters. The age of leptocephali was estimated by counting daily growth increments. Age of early metamorphosing leptocephali at recruitment to the estuary ranged from 155 to 183 days, indicating that migration of conger eel leptocephali from their oceanic spawning ground to the estuary requires 5–6 months. Back-calculated hatching dates suggest that the spawning season lasted 3 months, from late October to mid-December. However, in the late metamorphic leptocephali, the presence of an unclear peripheral zone in the otolith prevents the accurate estimation of the larval stage duration. The calcium content was almost constant throughout the otoliths. Both strontium and Sr:Ca ratios increased with age, but dramatically decreased at age 70–120 days. The otolith increment width also showed a marked increase at the same ages, indicating the onset of metamorphosis. A negative correlation between age at metamorphosis and otolith growth rate indicates that faster growing leptocephali arrive at the estuary earlier than slower growing ones. A close relationship was also found between age at recruitment and age at metamorphosis, suggesting that individuals that metamorphosed earlier were recruited to the estuary at a younger age. This larval migration pattern appears to be similar among anguilliform fishes.Communicated by S.A. Poulet, Roscoff     

Variation in migratory history of Japanese eels,<Emphasis Type="Italic"> Anguilla japonica</Emphasis>, collected in coastal waters of the Amakusa Islands,Japan, inferred from otolith Sr/Ca ratios

In order to examine the variation in migratory history of the Japanese eel, Anguilla japonica, we measured otolith strontium (Sr) and calcium (Ca) concentrations by X-ray electron microprobe analysis in 5 yellow eels and 20 silver eels collected in the coastal waters of the Amakusa Islands during the spawning migration season. Three migratory types categorized as river eels, estuarine eels and sea eels were found. Estuarine eels were dominant (52%), sea eels were the second most abundant (28%), followed by river eels (20%). The low proportion of river eels from the spawning migration season suggested that the estuarine and sea eels that inhabit the nearby coastal areas might make a larger reproductive contribution to the next generation in this area, although similar analyses should be made over the wide-range geographic distribution of this species, to provide better estimates of the reproductive contributions by different migratory patterns of the population.     

Distribution and early life history of <Emphasis Type="Italic">Kaupichthys</Emphasis> leptocephali (family Chlopsidae) in the central Indonesian Seas

Leptocephali of the widely distributed tropical marine eels of the genus Kaupichthys (family Chlopsidae) were collected around Sulawesi Island during a sampling survey in the Indonesian Seas in late September and early October 2002, and the otolith microstructure of 24 of the 59 specimens captured was examined to learn about the larval growth rates and spawning times of these small sized eels. Leptocephali ranging in size from 25 to 60 mm were collected in Makassar Strait and the Celebes Sea, but they were most abundant in the semi-enclosed Tomini Bay of northeast Sulawesi Island. The Kaupichthys leptocephali examined had 39–161 otolith growth increments. Their back-calculated hatching dates indicated that five age groups were present and each group appeared to have been spawned around the full moon of previous months. Average growth rate estimates of the first two age groups were 0.65 and 0.54 mm/day for the 27.4–30.4 and 37.6–45.6 mm age classes. The growth rates of the oldest three age groups (52.0–60.8 mm) appeared to have slowed down after they reached their approximate maximum size. An increase in increment widths at the outer margin of the otoliths of those larger than 53 mm suggested that the process of metamorphosis had begun even though there were few external morphological changes indicating metamorphosis. It is hypothesized that chlopsid leptocephali have an unusually short gut that may not need to move forward during early metamorphosis. The presence of four age classes in Tomini Bay suggests that the Togian Islands region may be productive habitats for Kaupichthys juveniles and adults.     

Relationship between growth rate and age at recruitment ofAnguilla japonica elvers in a Taiwan estuary as inferred from otolith growth increments

The growth history and recruitment dynamics of eel (Anguilla japonica) elvers were studied. Observations were based on growth increments in sagittal otoliths of elvers collected from Shuang-Chi River estuary off northeastern Taiwan, from November 1985 to February 1986. Total lengths of elvers upon arrival at the estuary were similar in most case; mean total lengths were from 55.99 to 59.06 mm. Daily ages of elvers at arrival ranged from 112.8±9.4 (±SD) to 156.5±13.5 d, indicating that migration of eel larvae from their oceanic spawning ground to the estuary requires 4 to 5 mo. Elver hatching dates, back-calculated from estimated daily ages, indicated that the spawning season lasted 5 mo (from late June to early October). Furthermore, the earlier eels spawned, the earlier elvers reached the estuary. The transition in growth history during the larval stage was obvious, as indicated from the change in increment width in elver otoliths. The inverse correlation between daily age and mean daily growth rates of fish length and otolith indicated that the age of elvers upon arrival at the estuary was susceptible to larval growth rate. In other words, the time taken on migration from oceanic spawning ground to the estuary was shorter for fast-growing larvae than for slowgrowing ones.     

Early life history of tropical Anguilla leptocephali in the western Pacific Ocean

In order to examine the early life-history characteristics of tropical eels, otolith microstructure and microchemistry were examined in leptocephali of Anguilla bicolor pacifica (27.6-54.1 mm TL, n=20) and A. marmorata (22.0-47.3 mm TL, n=8) collected during a cruise in the western Pacific. A. bicolor pacifica occurred between 10°N and 15°N in the west and between 5°S and 10°N farther to the east. A. marmorata also occurred in two different latitudinal ranges in the Northern (15-16°N) and Southern Hemispheres (3-15°S) of the western Pacific. The increment widths in the otoliths of these leptocephali increased between the hatch check (0 days) and about an age of 30 days in both species, and then gradually decreased toward the otolith edge. Otolith Sr:Ca ratios showed a gradual increase from the otolith center to the edge. The ages of A. bicolor pacifica and A. marmorata leptocephali ranged from 40 to 128 days and from 38 to 99 days, respectively. Growth rates of A. bicolor pacifica and A. marmorata leptocephali ranged from 0.33 to 0.71 mm day^-1 and from 0.45 to 0.63 mm day^-1, respectively. These leptocephali had estimated growth rates that were spread out throughout most of the reported range of growth rates of the leptocephali of the temperate species, the Japanese eel and the Atlantic eels. Differences in the spatial distribution in relation to current systems, and the age and size compositions of the leptocephali of A. bicolor pacifica and A. marmorata suggested different spawning locations for these two species.     

Early life history and recruitment of the tropical eel Anguilla bicolor pacifica, as revealed by otolith microstructure and microchemistry

Otolith microstructure and microchemistry of the tropical eel Anguilla bicolor pacifica Schmidt were examined in glass eels collected at the mouth of the Dumoga River, North Sulawesi Island, Indonesia. Ages of the glass eels examined (age at recruitment) ranged from 124 to 202 d (167 ± 19.3 d; mean ± SD), hatching being estimated as having occurred between November 1995 and March 1996. Otolith increment widths markedly increased from age 101 to 172 d (135 ± 18.2 d; mean ± SD), coincident with a drastic decrease in otolith Sr:Ca ratios, suggesting that metamorphosis began during that period. The duration of metamorphosis was estimated as 20 to 40 d, on the basis of otolith microstructural characteristics. The fluctuation patterns in otolith increment widths and Sr:Ca ratios were similar to those of the temperate Japanese eel A. japonica. Received: 20 May 1998 / Accepted: 7 October 1998     

Temperature-dependent recruitment delay of the Japanese glass eel <Emphasis Type="Italic">Anguilla japonica</Emphasis> in East Asia

Japanese eels spawn mainly during June–August. The larvae (leptocephali) then drift for 3–5 months before metamorphosing into glass eels. The recruitment season generally starts in southern East Asia in November and in northern areas in April the following year, a lag of ~5 months. However, analysis of otolith daily growth rings revealed only a 1–2-month difference in the mean leptocephalus stage between southern and northern East Asian samples. Experiments and field observation indicate that glass eels may starve, lose body weight, and remain in early pigmentation stage for a few months in cold waters. The time lag in recruitment can be accounted for by a longer leptocephalus stage combined with a low temperature-driven delay to upstream migration in winter. The leptocephalus duration and oceanic currents determine the dispersal locations up to the glass eel phase, while temperatures determine the timing of upstream migration time at each location.     

Climatic effects on the growth of a temperate reef fish from the Southern Hemisphere: a biochronological approach

Increments in the hard parts of marine organisms (otoliths, skeletons, shells) can provide long-term chronologies of growth analogous to tree rings. For the first time in the Southern Hemisphere, we use a dendrochronological (tree-ring analysis) approach to develop a multidecadal chronology of growth for a temperate reef fish, Girella tricuspidata, from the coast of northern New Zealand. Growth patterns in the otoliths of this species were strongly synchronous among individual fish over a period spanning 27 years (1980–2006). We then compared our otolith chronology to climatic records and found strong positive correlations of growth with sea surface temperature, and weak negative correlations with the multivariate El Nino Southern Oscillation (ENSO) index. Strongest correlations were found between summer sea surface temperature and otolith growth. This relationship was consistent across all years and explained 44 % of the variation (y = −2.0 + 0.1785 × temperature, r ² = 0.4367, P = 0.0002) in the G. tricuspidata growth chronology. Our study illustrates how otolith chronologies provide remarkable records of annual growth patterns over decadal time scales that will be useful for forecasting the likely effects of climate change on marine ecosystems.     

Swimming ability of eels (<Emphasis Type="Italic">Anguilla rostrata,Conger oceanicus</Emphasis>) at estuarine ingress: contrasting patterns of cross-shelf transport?

The transport of eel early life stages may be critical to their population dynamics. This transport from ocean spawning to freshwater, estuarine and coastal nursery areas is a combination of physical and biological processes (including swimming behavior). In New Jersey, USA, the American eel (Anguilla rostrata) enters estuaries as glass eels (48.7–68.1 mm TL) in contrast to the Conger eel (Conger oceanicus) that enters as larger (metamorphosing) leptocephali (68.3–117.8 mm TL). To begin to understand the mechanisms of cross-shelf transport for these species, we measured the potential swimming capability (critical swimming speed, U _crit) under ambient conditions throughout the ingress season. A. rostrata glass eels were collected over many months (January–June) at a range of temperatures (4–21°C), with relative condition declining over the course of the ingress period as temperatures warmed. C. oceanicus occurred later in the season (April–June) and at warmer temperatures (14–24.5°C). Mean U _crit values for A. rostrata (11.7–13.3 cm s⁻¹) and C. oceanicus (14.7–18.6 cm s⁻¹) were comparable, but variable, with portions of the variability explained by water temperature, relative condition, ontogenetic stage, and fish length. Travel times to Little Egg Inlet, New Jersey, estimated using 50% U _crit values, indicate it would take A. rostrata ~30 and ~60 days to swim from the shelf edge and Gulf Stream, respectively. Travel times for C. oceanicus were shorter, ~20 days from the shelf edge, and ~45 days from the Gulf Stream. Despite differences in life stage, our results indicate both species are competent swimmers, and suggest they are capable of swimming from the Gulf Stream and/or edge of the continental shelf to estuarine inlets.     

Changes in otolith microstructure and microchemistry during larval development of the European conger eel (<Emphasis Type="Italic">Conger conger</Emphasis>)

Otolith microstructure and chemical composition (Sr:Ca ratios) of the European conger eel (Conger conger) were examined during the larval developmental stages by scanning electron microscopy and wavelength dispersive spectrometer. Back-calculated hatching dates from the otolith microstructure of the developing leptocephali indicate a protracted spawning season from December to June. The early age of our developing specimens captured south of the Azores Islands suggests that the conger eel has another spawning area closer to Azores than the Mediterranean. Otolith increment width, which was relatively constant and narrow in the developing leptocephalus stage, increased sharply at age 170-250 days. Sr:Ca ratios in the otolith, which increased during the developing leptocephalus stage, showed a rapid drop coinciding with the increase in increment width. These coincidental changes were regarded as the onset of metamorphosis for this species. A close linear relationship between the age at metamorphosis and otolith growth rate indicates that the faster-growing larvae metamorphose earlier, suggesting that somatic growth should play an important role in the timing of metamorphosis. As shown in earlier work, the existence of an otolith marginal zone with unclear rings during metamorphosis prevents an accurate estimate of the larval stage duration of this species.     

Dietary effects on multi-element composition of European eel (<Emphasis Type="Italic">Anguilla anguilla</Emphasis>) otoliths

Otolith microchemistry is widely used as a tool to track individual migration pathways of diadromous fish under the assumption that the elemental composition of fish otoliths is directly influenced by the physicochemical properties of the surrounding water. Nevertheless, several endogenous factors are reported to affect element incorporation into fish otoliths and might lead to misinterpretations of migration studies. This study experimentally examined the influence of eight different diets on the microchemical composition of European eel (Anguilla anguilla) otoliths using laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS). Seven natural prey types and one artificial diet were fed during 8 weeks in freshwater circuits. Results show for the first time that food has no significant influence on the incorporation of Na, Sr, Ba, Mg, Mn, Cu and Y into European eel otoliths. This indicates that the incorporation of elements usually chosen for migration studies is not affected by diet and that individual feeding behaviour of A. anguilla will not lead to any misinterpretation of migration pathways.     

Orientation mechanisms in migrating European silver eel (Anguilla anguilla): Temperature and olfaction

The migration pattern of silver eel (Anguilla anguilla L.) in the Baltic is well documented from many tagging experiments. This particular investigation differed from previous taggings in that the background of all the eels used was the same. They came from a 1980 stocking programme and had been imported from France as glass eels. When migrating these stocked eels missed the outlet of the Baltic and continued in a south-westerly direction. They were still reported in this southern-most area more than 4 yr later. Indigenous eels turn northwards after passing the south of Sweden and leave the Baltic through the narrow Sound. Since the formerly stocked eels had never been in the Baltic, the absence of an imprinted olfaction cue may explain their orientation failure. Although lacking an imprinted olfaction cue eels were recaptured mainly in a very restricted area in the southwestern Baltic. This reflects another cue, genetic or imprinted during the Atlantic journey. This second cue, temperate, can also serve as the trigger which causes eels to stop migrating and to initiate spawning. The enclosed Baltic acts as a giant trap for eels from the huge stocking programmes undertaken there. As a consequence stocked eels probably contribute little to spawning stocks in the Sargasso Sea which may have contributed to the decrease in abundance of glass eels reported from western Europe in recent decades.     

Ontogenic change of gill chloride cells in leptocephalus and glass eel stages of the Japanese eel, <Emphasis Type="Italic">Anguilla japonica</Emphasis>

The development of gill chloride cells was examined in premetamorphic larvae (leptocephali) and juveniles (glass eels) of the Japanese eel, Anguilla japonica. Branchial chloride cells were detected by immunocytochemistry using an antiserum specific for Na⁺,K⁺-ATPase. The specificity and availability of the antiserum for the detection of Japanese eel chloride cells were confirmed by Western blot analysis. The chloride cells first appeared on the developing gill filaments in a mid larval stage of leptocephalus (32.2 mm). Both immunoreactivity and the number of chloride cells gradually increased as the fish grew to a late stage of leptocephalus over 54 mm. In glass eels just after metamorphosis, gill lamellae developed from the gill filaments, and a rich population of chloride cells was observed in the gill filaments. In glass eels collected at a coastal area, chloride cells were extensively distributed in the gill filaments. The chloride cell size decreased progressively in glass eels transferred from seawater (SW) to freshwater (FW), whereas there was no difference in cell number. In contrast, some Na⁺,K⁺-ATPase immunoreaction distinct from typical chloride cells was observed in the gill lamellae throughout FW-transferred fish, but disappeared in control fish maintained in SW for 14 days. These findings indicate that the gill and gill chloride cells developed slowly during the extremely long larval stage, followed by rapid differentiation during a short period of metamorphosis. The excellent euryhalinity of glass eels may be due to the presence of the filament chloride cells and lamellar Na⁺,K⁺-ATPase-immunoreaction, presumably being responsible for SW and FW adaptation, respectively.     

Metabolic response under different salinity and temperature conditions for glass eel Anguilla japonica

Diadromous fish often enter freshwater directly from seawater via fish ladders or channels built in estuarine dams. The oxygen consumption rates (OCR) of glass eel, Anguilla japonica, were determined using an automatic intermittent flow respirometer under various salinity and temperature regimes to physiologically explain this direct movement. The endogenous rhythm of the OCR in wild glass eels, freshly collected from estuaries, was nearly synchronous with the tidal pattern at the estuarine collection site. When the salinity was changed from 20 psu (12°C) at a constant temperature to that of freshwater, the OCR of the glass eels decreased by 21.6±7.0% (mean ± SD) (P<0.05), showing a dampened rhythm for about 48 h. After this period of impediment, the glass eels resumed normal metabolic activity. Direct migration from seawater to freshwater under constant temperature would result in a severe physiological stress for these glass eels for about two days. When the glass eels were exposed to a cyclic change in water temperature of 2°C 26 h⁻¹, as they encounter in estuaries, and then were introduced to freshwater abruptly, the OCR rhythm corresponded to the cyclic changes in water temperature after exposure to freshwater. Under these conditions, the mean OCR of the glass eels had a small difference before and after exposure to freshwater. These data explained how glass eels can directly move from sea water into the freshwater without any apparent metabolic stress in the estuaries showing cyclic change in water temperature (Δt=2°C).     

Microstructural growth in otoliths of conger eel (Conger myriaster) leptocephali during the metamorphic stage

Otolith growth during metamorphosis and some aspects of the early life history of conger eel (Conger myriaster) were determined as indicated from microstructure in otoliths of the leptocephali collected from Cheonsu Bay, Korea during May and June 1988. The leptocephali occurred from early May to late June in the study area. Larvae collected in early May were in the late leptocephalus stage, and the proportion of the metamorphosing leptocephali increased over time. Otoliths in the late leptocephalus stage showed a translucent zone only. Although the fish did not feed and the body length diminished during metamorphosis, the otolith continued to grow and, consequently, the opaque zone was formed outside the translucent zone. The inner translucent zone can be considered a leptocephalus zone, and the outer opaque zone a metamorphic zone. Assuming that the growth increments were deposited daily from hatching, the conger eel can be considered to have hatched between September and February. The number of increments in the inner hyaline zone ranged from 124 to 239, and was assumed to represent the number of days from hatching to the onset of metamorphosis. The duration of metamorphosis was estimated as 51 to 75 d based on the number of increments in the opaque zone at the end of the metamorphic stage.     

Occurrence of the semi-catadromous European eel Anguilla anguilla in the Baltic Sea

Strontium (Sr) and calcium (Ca) contents in the otoliths of yellow and silver European eels [Anguilla anguilla (L.)] collected from coastal waters of the Baltic Sea and a freshwater lake in Sweden were examined by wavelength dispersive X-ray spectrometry with an electron microprobe. The mean Sr/Ca ratios from elver check to otolith edge were significantly higher for the eels from coastal waters (5.39 ± 1.09‰) than for those from the lake (0.71 ± 0.89‰). The evidence indicates that European eels in the Baltic Sea do not necessarily migrate into freshwater streams during the growth phase. Received: 30 September 1999 / Accepted: 6 April 2000     

Stable isotope analysis of two species of anguilliform leptocephali (<Emphasis Type="Italic">Anguilla japonica</Emphasis> and <Emphasis Type="Italic">Ariosoma major</Emphasis>) relative to their feeding depth in the North Equatorial Current region

Anguilla japonica leptocephali are transported from their offshore spawning area to their recruitment areas in East Asia, but their depth distributions, food sources and feeding are still poorly known. This study analyzed carbon and nitrogen stable isotope ratios of leptocephali of A. japonica, Ariosoma major and Ariosoma spp., and of particulate organic matter (POM), their likely food source, at five different depths in 2004–2009. We used mixing models to show that A. japonica appeared to be feeding at depths between 5 and 50 m, but sometimes deeper. A. major appeared to have a tendency of mostly feeding at depths of 50 m or shallower. Although the A. japonica and Ariosoma spp. collected in the same area during the leptocephalus stage appeared to have different feeding ecologies possibly related to different types of POM, their different depth distributions, sizes and transport histories may also help explain these differences.     

New clues for freshwater eels (<Emphasis Type="Italic">Anguilla</Emphasis> spp.) migration routes to eastern Madagascar and surrounding islands

A total of 4,172 freshwater eels have been collected by electrofishing in upper estuaries from Madagascar (East coast), Mascarene (Réunion and Mauritius Is.), Comoros (Mayotte Is.) and Seychelles (Mahé and Praslin Is.) Archipelagos, between October 2003 and February 2006. Eel species composition in the sampling stations was contrasted between eastern Madagascar (Anguilla mossambica 96.0%, A. marmorata 3.9% and A. bicolor bicolor 0.2%), the Comoros (A. marmorata 56.1% and A. bicolor bicolor 43.9%), the Mascarene (A. marmorata 91.4%, A. bicolor bicolor 5.4% and A. mossambica 3.2%) and the Seychelles Archipelagos (A. bicolor bicolor 100.0%). This gradient in species composition, even concerning the short time-range of our sampling, argued for separate migration routes between species. A total of 168 eels were aged by reading their otolith microstructure, and otolith growth rates were calculated from pre-leptocephalus stage (post-hatching) to metamorphosis, until freshwater check. For all species, mean otolith growth rate (OGR) was related to specific migration routes: A. bicolor bicolor is distributed in the lowest latitudes and showed the highest OGR during leptocephalus stage, whereas A. mossambica, endemic of the Malagasy area, has the most southern distribution and showed the lowest OGR. OGR during leptocephalus stage was negatively correlated to the leptocephalus stage duration, showing a decrease of global metabolism with time, classical in leptocephali. This relationship was found significant for A. marmorata and A. mossambica, probably because all these larvae crossed successively the same environments, but not for A. bicolor bicolor, probably because their larvae crossed different pelagic environments, opening the hypothesis of larvae from different origins.