Tropical Eels Research Articles

Timing of maturation of a tropical eel, Anguilla bicolor bicolor in Malaysia

Summary In order to understand the life history of the tropical freshwater eel Anguilla bicolor bicolor found in Malaysian natural waters, the timing of maturation was studied. Age at maturation of the species ranged from 4 to 6 years. The timing of maturation was similar to that of the temperate eel A. japonica, but earlier than that of other temperate eels A. anguilla, A. rostrata, A. australis and A. dieffenbachii, reported previously. The higher growth rate found in A. bicolor bicolor associated with the habitat environment might induce the differences in the maturation timing among species.

Morphological and physiological changes of female tropical eels, Anguilla celebesensis and Anguilla marmorata, in relation to downstream migration

The morphological and physiological characteristics of migrating and non-migrating female tropical eels, Anguilla celebesensis and Anguilla marmorata were examined in relation to their downstream migration on central Sulawesi Island, Indonesia. Migrating eels (64 A. celebesensis and 37 A. marmorata) were obtained from weirs set near the outlet area of Poso Lake and non-migrating eels (21 A. celebesensis and 21 A. marmorata) were sampled by set-lines and eel pots in Poso Lake, its inlet rivers, and in the La River system during February 2009 to October 2010. In both species, values of eye index, pectoral-fin length index, gonado-somatic index (I(G)), hepato-somatic index, swimbladder-somatic index and cardio-somatic index of migrating eels were significantly higher than those of non-migrating eels and the gut-somatic index values of the migrating eels were significantly lower than that of non-migrating eels. When silvering stages of eels were classified by the silvering index for Anguilla japonica, in A. celebesensis, all non-migrating eels were Y1 stage and the migrating eels consisted of Y2, S1 and S2 stages eels. In A. marmorata, the non-migrating eels consisted of Y1 and Y2 eels, and the migrating eels consisted of Y2 and S1 eels, but there were no S2 eels. Results of principal component analysis (PCA) of morphological and physiological variables suggested that these characteristics changed drastically between the Y1 and Y2 stages in A. celebesensis, while A. marmorata showed a gradual change with silvering, which differs from the temperate species A. japonica. The mean ±S.D. I(G) value of migrating A. celebesensis (6.9 ± 1.8, 3.3-11.4) was very high and that of A. marmorata (3.1 ± 0.8, 1.8-5.7) was comparatively low. The very different rates of maturation that were found between these two species provide support for the hypothesis that the reproductive characteristics of silver eels can reflect their migration scale.

Lipid Class and Fatty Acid Content of the Leptocephalus Larva of Tropical Eels

The leptocephalus larva of eels distinguishes the elopomorph fishes from all other bony fishes. The leptocephalus is long lived and increases in size primarily through the synthesis and deposition of glycosaminoglycans. Energy stored during the larval stage, in the form of glycosaminoglycan and lipids, is required to fuel migration, metamorphosis and metabolism of the subsequent glass eel stage. Despite the importance of energy storage by leptocephali for survival and recruitment, their diet, condition and lipid content and composition is essentially unknown. To gain further insight into energy storage and condition of leptocephali, we determined the lipid class and fatty acid concentration of larvae collected on a cross-shelf transect off Broome, northwestern Australia. The total lipid concentration of two families and four sub-families of leptocephali ranged from 2.7 to 7.0 mg g wet weight(-1), at the low end of the few published values. Phospholipid and triacylglycerol made up ca. 63 % of the total lipid pool. The triacylglycerol:sterol ratio, an index of nutritional condition, ranged from 0.9 to 3.7, indicating that the leptocephali were in good condition. The predominant fatty acids were 16:0 (23 mol%), 22:6n-3 (docosahexaenoic acid, DHA, 16 mol%), 18:0 (8.2 mol%), 20:5n-3 (eicosapentaenoic acid, EPA, 6.7 mol%), 18:1n-9 (6.4 mol%) and 16:1n-7 (6.3 mol%). The DHA:EPA ratio ranged from 2.4 to 2.9, sufficient for normal growth and development of fish larvae generally. The leptocephali had proportions of bacterial markers >4.4 %, consistent with the possibility that they consume appendicularian houses or other marine snow that is bacteria rich.

Evolution of Microsatellite Loci of Tropical and Temperate Anguilla Eels

Anguilla eels are divided into temperate and tropical eels, based on their major distributions. The present study collected two temperate eels, Anguilla japonica and Anguilla anguilla, and two tropical eels, Anguilla marmorata and Anguilla bicolor pacifica, to examine two questions: do temperate and tropical Anguilla eels have different genetic polymorphic patterns?; and do temperate Anguilla japonica and Anguilla anguilla have a closer relationship to each other than to tropical eels? In total, 274 sequences were cloned and sequenced from six conserved microsatellite loci to examine polymorphic patterns of these four catadromous eels. Different mutational events, including substitutions, and repeat-unit deletions and insertions, appeared in major regions, while different point mutations were observed in flanking regions. The results implied that parallel patterns of microsatellite sequences occurred within both tropical and temperate freshwater eels. Consensus flanking sequences of six homologous loci from each of the four species were constructed. Genetic distances ranged from 0.044 (Anguilla bicolor pacifica vs. Anguilla marmorata) to 0.061 (Anguilla marmorata vs. Anguilla anguilla). The tree topology suggests the hypothesis of Anguilla japonica and Anguilla anguilla being a sister group must be rejected.

Notes on the occurrence of the tropical eel Anguilla bicolor bicolor in Peninsular Malaysia, Malaysia

Previous studies indicated that a tropical freshwater eel Anguilla bicolor bicolor occurs in Africa, India, Sri Lanka, Bangladesh, Myanmar, Indonesia and Australia, but an intensive survey has indicated an extended distribution range for the species into Peninsular Malaysia. Thus, A. b. bicolor is a native subspecies of Malaysia.

Phylogeography of Anguilla marmorata (Teleostei: Anguilliformes) from the eastern Caroline Islands

Recent analyses of the tropical giant mottled eel Anguilla marmorata have suggested four to six populations within its Indo-Pacific distribution, including one represented by specimens from Guam, and that the population on Guam includes eels occurring in the eastern Caroline Islands based on morphological similarities. To test this hypothesis, sequences of the entire mitochondrial control region (mtCR) were obtained for 39 eels from Kosrae and Pohnpei, and compared to 267 previously sequenced haplotypes from across the Indo-Pacific Ocean. Results support recognition of two lineages distinctive for the eastern Caroline Islands and Guam, and the likelihood of an additional spawning area in the Indo-Pacific Ocean.

Present and past genetic connectivity of the Indo‐Pacific tropical eel Anguilla bicolor

AbstractAim The objective of this study was to reveal the present population structure and infer the gene‐flow history of the Indo‐Pacific tropical eel Anguilla bicolor.Location The Indo‐Pacific region.Methods The entire mitochondrial control region sequence and the genotypes at six microsatellite loci were analysed for 234 specimens collected from eight representative localities where two subspecies have been historically designated. In order to infer the population structure, genetic differentiation estimates, analysis of molecular variance and gene‐tree reconstruction were performed. The history of migration events and population growth was assessed using neutrality tests based on allelic frequency spectrum, coalescent‐based estimation of gene flow and Bayesian demographic analysis using control region sequences.Results Population structure analysis showed genetic divergence between eels from the Indian and Pacific oceans (FST = 0.0174–0.0251, P < 0.05 for microsatellites; ΦST = 0.706, P < 0.001 for control region), while no significant variation was observed within each ocean. Two mitochondrial sublineages that do not coincide with geographical regions were found in the Indian Ocean clade of a gene tree. However, these two sublineages were not differentiated at the microsatellite markers. The estimation of mitochondrial gene‐flow history suggested allopatric isolation between the Indian and Pacific oceans, and a possible secondary contact within the Indian Ocean after an initial population splitting. Bayesian demographic history reconstruction and neutrality tests indicated population growth in each ocean after the Indo‐Pacific divergence.Main conclusions Anguilla bicolor has diverged between the Indian and Pacific oceans, which is consistent with the classical subspecies designation, but is apparently genetically homogeneous in the Indian Ocean. The analysis of gene‐flow and demographic history indicated that the two mitochondrial sublineages observed in the Indian Ocean probably represent the haplotype groups of relict ancestral populations. A comparison with a sympatric congener suggested that absolute physical barriers to gene flow may not be necessary for population divergence in eels.

Analysis of vertebral counts of the tropical anguillids, Anguilla megastoma, A. obscura, and A. reinhardtii, in the western South Pacific in relation to their possible population structure and phylogeny

The population structures of three tropical eel species, Anguilla megastoma, A. obscura, and A. reinhardtii, collected from several localities of each species range in the western South Pacific Ocean were evaluated using statistical analyses of total number of vertebrae (TV) data, which also included previously published data. There was a significant difference in TV values between Samoa and French Polynesia specimens of A. megastoma, while no significant difference was observed in TV data of A. obscura, despite the two species having similar overlapping species distribution ranges. There also was no significant difference found in the TV data of A. reinhardtii. These results suggest that A. megastoma may be separated into eastern and western populations in the western South Pacific, but there was no statistical evidence using the TV data that A. obscura and A. reinhardtii have population structure in the western South Pacific. These possible types of population structures are discussed in relation to the phylogeography and life histories of other tropical anguillid eels.

Habitat use and habitat transitions in the tropical eel, Anguilla bicolor bicolor

Recently, the migratory history of temperate species of anguillid eels has been intensively studied using analytical microchemical techniques to determine the ratios of strontium to calcium (Sr:Ca) in the otoliths. However, there have been few studies of this nature on tropical anguillid eel species. To elucidate the migration ecology of the freshwater eel genus Anguilla, as well as its life history and habitat use, we examined the otolith Sr and Ca concentrations of a tropical anguillid eel Anguilla bicolor bicolor collected in Indonesian waters. In A. bicolor bicolor collected in a lagoon area, the change in Sr:Ca ratios outside the high Sr:Ca core showed two patterns of habitat use, (1) constantly living in either brackish or sea waters with no freshwater life (residents, 37%), and (2) habitat shift from freshwater to brackish or sea waters (migrants, 63%). For migrant fishes, most fish shifted their residence between 520 and 950 μm (mean: 740 μm) from the otolith core. These transitions suggest that these specimens moved to a higher salinity environment. The wide range of otolith Sr:Ca ratios (0.02 × 10−3 to 12.79 × 10−3 in all analytical points outside of 150 μm from the core of all otoliths) in A. bicolor bicolor indicated that the habitat use of the tropical eel was facultative among fresh, brackish and marine waters during their growth phases after recruitment to the coastal areas. This flexible habitat use was the same as that of temperate eels. Thus, the migrations of anguillid eels into freshwater is clearly not an obligatory behavior.

Investigation of tropical eel spawning area in the South-Western Indian Ocean: Influence of the oceanic circulation

In the South-Western Indian Ocean (SWIO), four eel species of the genus Anguilla (i.e. Anguilla bicolor bicolor, Anguilla nebulosa labiata, Anguilla marmorata and Anguilla mossambica) were identified, while their respective oceanic spawning area remained unknown. Based on collected larvae, glass eel captures and hydrodynamical conditions, previous studies raised the hypothesis that the eel spawning area might be common to all of those freshwater eel species, and located East of Madagascar. An original modeling approach, based on backward simulations, is developed to assess how the ocean circulation in the SWIO determines the location of the spawning areas and whether a common spawning area for each recruitment site where glass eels were found is possible. We use a hydrodynamical model, which reproduces realistically the 3D open ocean circulation in the region, associated with a Lagrangian model that calculates the possible migration pathways of larvae, represented by passive particles. Some biological parameters, provided by previous otolith microstructures analysis, are taken into account to constrain our simulations. Results suggest the existence of a common spawning area located between 13°S and 19°S and westwards of 60.5°E, although these boundaries vary on the interannual timescale. Salinity fronts were reported beside the boundaries, reinforcing this assumption. We explore the impact of hydrodynamic conditions on recruitment and migration durations from three specific regions within the common spawning area. They all allow migration to each recruitment sites consistent with duration estimated from otolith microstructure analyses. Nevertheless, there is substantial variability on intra-seasonal to interannual timescale in simulated migration durations and arrival success, with specific amplitude to each recruitment site and spawning location.

Occurrence of marine resident tropical eel Anguilla bicolor bicolor in Indonesia

In order to understand the migratory history and habitat use of the tropical anguillid eels Anguilla celebesensis, A. marmorata, and A. bicolor bicolor, the otolith strontium (Sr) and calcium (Ca) concentrations were examined for eels collected in Indonesian waters. In A. bicolor bicolor collected in a lagoon, the change in Sr:Ca ratios outside the high Sr:Ca core generally indicated two patterns of habitat residence: (1) constant living in either brackish or sea waters with no freshwater life (25%) and (2) habitat shifts from fresh water to brackish or sea waters (75%). No A. bicolor bicolor had a general life history as a freshwater resident. A. celebesensis and A. marmorata from the uppermost freshwater lake showed freshwater life history patterns. The wide range of otolith Sr:Ca ratios in A. bicolor bicolor indicated that the habitat use of this tropical eel was facultative among fresh, brackish, and marine waters during the growth phase after recruitment to coastal areas similar to that for temperate eels. Thus, the migration of anguillid eels into fresh water is clearly not an obligatory.

Sympatric spawning of Anguilla marmorata and Anguilla japonica in the western North Pacific Ocean

Extensive collections were made of the larvae of the temperate Japanese eel Anguilla japonica and the tropical giant mottled eel Anguilla marmorata in an overlapping area of the North Equatorial Current region of the western North Pacific Ocean. Collections of 189 A. marmorata and > 2500 A. japonica larvae during nine surveys from 1991 to 2007 showed that these two anguillid eels have similar spawning areas just west of the southern West Mariana Ridge. In July to August 2006 and August 2007, morphologically and genetically identified A. marmorata preleptocephali were mainly collected between 14.5-15 degrees N and 142-142.5 degrees E, where A. japonica preleptocephali were also caught in some of the same net tows. Fewer A. marmorata preleptocephali, however, were collected (n = 31) compared to those of A. japonica (n = c. 165), and fewer small larvae of A. marmorata were collected per tow than A. japonica (n = 1-10 and 1-294, respectively), suggesting relatively smaller spawning aggregations of A. marmorata. The distribution of preleptocephali and small larvae was wider in longitude in A. marmorata (131- 143 degrees E) than in A. japonica (137-143 degrees E), while the latitudinal range was almost the same (12-17 degrees N). Although spawning by these two species overlaps both spatially and temporally, the tropical eels of the North Pacific population of A. marmorata probably have a much longer spawning season with fewer spawners, at least in summer, and recruit to a much wider latitudinal range of growth habitats.

Heavy Metals in a Tropical Eel Anguilla marmorata from The Central Part of Vietnam

In order to understand the present status of heavy metal contamination and the risk associated with human consumption, commercial freshwater eels in Vietnam were examined. The concentration of eight elements (Cr, Mn, Co, Cu, Zn, Sr, Cd, and Pb) was determined in muscle tissue of tropical eel Anguilla marmorata collected in four provinces, Quang Tri, Quang Ngai, Binh Dinh, and Phu Yen, from the central part of Vietnam. Concentrations of Cu, Zn, Cd, and Sr were found to be highest, whereas Co concentration showed the lowest at Quang Tri. Cr was recorded to be lowest in Quang Ngai, while the amounts of Mn and Pb did not vary among locations. Although the metal concentrations in the muscle of A. marmorata did not represent a risk for human consumption, elevated Cd concentrations in Quang Tri related to agriculture activities suggest that further investigations should be undertaken to clarify the potential risk to the eel population.

Seasonality of spawning by tropical anguillid eels around Sulawesi Island, Indonesia

Remarkably little is known about the life histories of the many tropical anguillid eels distributed across the Indo-Pacific region, and since the Danish expedition to study eels in the region in 1928 and 1929, research on these eels has only begun again in recent years. Sampling for anguillid leptocephali in the Indonesian Seas has been carried out recently to learn about the spawning ecology and larval distributions of tropical eels there. The leptocephali of Anguilla marmorata, Anguilla bicolor pacifica, Anguilla borneensis, Anguilla interioris, and Anguilla celebesensis were collected around Sulawesi Island both in May 2001 and October of 2002. The development of genetic identification techniques has enabled these leptocephali to be identified to species, and their distributions and sizes during different seasons indicated that there are differing life history patterns among sympatric species in the region. A. celebesensis was found to have been spawning in Tomini Bay of northeastern Sulawesi Island in March and April 2001, but apparently, no spawning had occurred in the late summer and fall of 2002. Studies on anguillid glass eels have suggested that tropical anguillids may spawn throughout much of year, but our research on leptocephali in Tomini Bay and data on the downstream migration of tropical anguillids in the major tributary to Tomini Bay indicate that A. celebesensis may have a distinct seasonal pattern of spawning possibly related to the regional monsoon cycles. This is the first evidence of seasonality of spawning in tropical anguillid eels whose life histories are only just beginning to be revealed.

Contrasts between spawning times of Anguilla species estimated from larval sampling at sea and from otolith analysis of recruiting glass eels

This study reviewed literature on spawning times for three north temperate species of anguillid eels estimated by sampling for small leptocephali (larvae) at sea and for several temperate and tropical species by back-calculating from putative daily ages derived from otolith increment analysis of glass eels that recruited to coastal waters. Estimates from otoliths of European eels, Anguilla anguilla, American eels, Anguilla rostrata, and Japanese eels, Anguilla japonica, imply much more protracted spawning seasons than are indicated by sampling at sea during various times of year. European eels are inferred to spawn year-round from otolith analysis, but the smallest, recently hatched leptocephali are found only in late winter and spring. From otoliths, the spawning times of these three species are all estimated to occur much later in the year than when small leptocephali are found at sea, indicating that ages appear to be underestimated. For these and other temperate and tropical eels, there are inconsistencies in assigned ages among various studies, which are most extreme for the European eel. This species has the longest larval migration and often has an opaque zone in the glass eels’ otoliths where it is difficult to discern growth increments. These inconsistencies suggest that interpretation of otolith growth increments is incorrect at least in some studies, and the apparently consistent mismatch between otolith and sea-sampling studies suggests that increments may not always be formed at some period during the unusual early life history of anguillids. Because daily increments may be formed in eels during most of their early life history, future research is needed to determine the cause of the mismatch of glass eel aging studies and the apparent spawning times of eels offshore.

Distribution and early life history of Kaupichthys 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.

Age and growth of Anguilla bicolor bicolor leptocephali in the eastern Indian Ocean

A sampling survey for leptocephali was conducted in the eastern Indian Ocean to the west of Sumatra from 5 to 20 June 2003 in an overlapping area with the historical survey in September to November 1929 during the Danish Round the World Expedition. The age and larval growth rate of 34 Anguilla bicolor bicolor collected in 2003 were estimated using their otolith microstructure to obtain new information about the early life history of this sub‐species. The total lengths and ages of these leptocephali were 44·1–55·5 mm and 114–158 days, respectively. Their hatching dates ranged from 3 January to 20 February 2003. Combining these age data and the estimated age of leptocephali collected by others in the same area, this sub‐species was estimated to have a wide range of spawning periods. Individual growth rates of the leptocephali in 2003 ranged from 0·32 to 0·39 mm day−1 with a mean ±s.d. of 0·35 ± 0·02 mm day−1. These values were lower than the growth rates of leptocephali of other tropical eels such as Anguilla celebesensis or Anguilla borneensis, suggesting that A. b. bicolor from the eastern Indian Ocean have a longer leptocephalus period of oceanic migration.

Distribution of leptocephali of the freshwater eels, genus Anguilla, in the waters off west Sumatra in the Indian Ocean

A research cruise was conducted in the eastern Indian Ocean off west Sumatra, Indonesia, in June 2003 to learn about the spawning and larval ecology of the tropical freshwater eels of the genus Anguilla in the region. A total of 43 anguillid leptocephali were collected during the cruise and they were genetically identified as 41 Anguilla bicolor bicolor, 1 Anguilla marmorata, and 1 Anguilla interioris. A. bicolor bicolor leptocephali were 44.1–55.5 mm TL and most of them were at the fully grown stage. Reexamination of the historical data of Jespersen (1942) also suggested a relatively low abundance of small size leptocephali (<40 mm) of this species off west Sumatra. Although the study area has long been considered to be a spawning site of A. bicolor bicolor, the distributions of leptocephali from the two surveys and the patterns of ocean currents in the region suggest the possibility that the main spawning area of this species is located farther offshore.

Contrasting patterns of growth and migration of tropical anguillid leptocephali in the western Pacific and Indonesian Seas

In order to improve understanding of the larval migration and early life history charac- teristics of 4 tropical eels, Anguilla marmorata, A. bicolor pacifica, A. celebesensis and A. borneensis, the leptocephali, metamorphosing leptocephali and oceanic glass eels collected during 8 cruises in the western Pacific and Indonesian Seas from 1991 to 2002 were analyzed. The leptocephali of A. celebesensis and A. borneensis were collected only in close proximity to their relatively small spe- cies ranges in the Indonesian Archipelago and were found to have faster growth than the other 2 species with small-scale local migrations. The more widely distributed species A. marmorata and A. bicolor pacifica were collected in most sampling areas. Small leptocephali of A. marmorata were collected only to the west of the Mariana Islands, and only larger specimens, metamorphosing leptocephali, or oceanic glass eels of both species were collected in the Indonesian Seas. These distributions suggested that the 2 species have intermediate-scale migrations compared to other anguillid eels. The leptocephali of all 4 species appeared to reach a fully grown size of around 50 mm, which is considerably smaller than the maximum size of temperate anguillid leptocephali, and their growth was predominantly faster than that of temperate species. These data and recently derived molecular phylogenetic relationships among all anguillid species in the world suggest that the long spawning migrations of temperate eels evolved from much shorter migrations of tropical species, whose larval growth was faster and whose maximum larval sizes were smaller.

Short-distance spawning migration of tropical freshwater eels.

The freshwater eels have fascinated biologists because of their spectacular long-distance migrations between their freshwater habitats and their spawning areas far out in the ocean (1, 2, 3). Recent progress on the molecular phylogeny of freshwater eels suggests that they originated in the tropics (4), and information on the reproductive ecology and recruitment of tropical species will provide new insight into the evolution of the spawning migration of the freshwater eels (5, 6). However, the larvae (leptocephali) of the many sympatric tropical species are morphologically similar (7), so they are impossible to identify, and their spawning areas are thus virtually unknown. Recently, however, we have collected small leptocephali from around Sulawesi, Indonesia, and have used species-specific genetic markers to identify them as larvae of Anguilla celebesensis and A. borne-ensis, which provides the first definitive information about the general spawning areas of these tropical eels. Moreover, the discovery of a spawning area of A. celebesensis in Tomini Bay and the presence of small specimens of two species in the Celebes Sea indicate that, in contrast to the long migrations made by temperate eels, tropical eels make much shorter migrations to spawn in areas near their freshwater habitats. This difference in migratory behavior may reflect an evolutionary cline among freshwater eels that extends from tropical to temperate regions.