Interspecific and sexual differences in riverine distribution of tropical eels Anguilla spp.

A total of 261 individuals of the four tropical eel species, Anguilla celebesensis, Anguilla marmorata, Anguilla bicolor pacifica and Anguilla interioris, were collected from 12 locations around Sulawesi Island, Indonesia, to gain knowledge about the riverine distribution of tropical eels. Anguilla marmorata was predominant in the lower reaches of Poso River (94·4% of total eel catch in the sampling area), Poso Lake (93·3%), three small inlet rivers of Tomini Bay (100%) and Laa River (92·3%). Anguilla celebesensis occurred frequently in the inlet rivers of Poso Lake (63·5%). Anguilla bicolor pacifica and Anguilla interioris were rare (1.5 and 0.4%, respectively). Otolith Sr:Ca ratio electron‐probe micro analysis (EPMA) for individual migratory histories revealed that 15 A. celebesensis caught in Poso Lake and its inlet rivers were categorized into 14 river eels (Sr:Ca < 2·5) showing upstream migration seemingly at their elver stage and only one sea eel (Sr:Ca ≥ 6·0) that stayed in the marine habitat for the majority of its life after recruiting to Sulawesi Island before its late upstream migration. In A. marmorata, 19 examined eels from Poso Lake and its inlet rivers were all river eels, while 17 eels from the lower reaches of Poso River were two river eels, six sea eels and nine estuarine eels (2·5 ≤ Sr:Ca < 6·0) that mostly lived in the brackish water. The sex ratio of A. celebesensis was highly skewed towards a dominance of females (99%). In A. marmorata, females were predominant in Poso Lake (95·2%), its inlet rivers (94·7%) and Laa River (100%), while males were more frequent in the lower reaches of Poso River (76·5%) and small inlet rivers of Tomini Bay (94·1%). These results indicate that the riverine distribution pattern of tropical eels differs among species and between sexes.     

Reassessment of age of sexual maturity in gibbons (hylobates spp.)

From studies of both wild and captive animals, gibbons are thought to reach sexual maturity at about 6 to 8 years of age, and the siamang (Hylobates syndactylus) at about 8 to 9 years. However, a review of the literature reveals that in most cases the exact age of the maturing animals was not known and had to be estimated. This study presents seven case reports on captive gibbons of known age. Captive males of the white-cheeked crested gibbon (H. leucogenys leucogenys) and of the siamang (H. syndactylus) can breed at the age of 4 and 4.3 years, respectively. Similarly, hybrid females (H. lar × H. moloch) and siamang females can breed at 5.1 and 5.2 years, respectively. This finding may help to improve the breeding success of captive gibbon populations. It is not clear whether gibbons reach sexual maturity earlier in captivity or whether sexual maturity is also reached by 5 years of age in the wild. Possible implications for the interpretation of group size regulation and of reproductive strategies of wild gibbons are discussed.     

A new species of Procamallanus (Nematoda: Camallanidae) from Pacific eels (Anguilla spp.)

A new species of parasitic nematode, Procamallanus (Procamallanus) pacificus n. sp., is described from the stomach of the Pacific shortfinned eel, Anguilla obscura (type host), and from the speckled longfin eel, Anguilla reinhardtii, from northern New Caledonia (Melanesia, South Pacific); from Anguilla sp. (cf. obscura) from the Fiji Islands (Melanesia, South Pacific); and from the giant mottled eel Anguilla marmorata from Futuna Island (Wallis and Futuna Islands, Polynesia). Although a total of 450 nematodes were collected, all specimens were females; this suggests either an extremely rare occurrence of males or parthenogenetic reproduction in this species. Procamallanus pacificus differs markedly from all congeners from fish hosts in possessing a greater number (4-9) of caudal mucrons in the female and by other morphological features. This parasite might become a serious pathogen of cultured eels in the region of the South Pacific. Batrachocamallanus Jackson and Tinsley, 1995 is considered a junior synonym of Procamallanus Baylis, 1923, to which 2 species are transferred as Procamallanus occidentalis (Jackson and Tinsley, 1995) n. comb. and Procamallanus siluranae (Jackson and Tinsley, 1995) n. comb. One third-stage larva of Procamallanus (Spirocamallanus) sp. was also recorded from Anguilla sp. (cf. obscura) from the Fiji Islands.     

Diel and seasonal movements of radio-tagged freshwater eels, Anguilla spp., in two New Zealand streams

We studied diel and seasonal movements of 21 radio-tagged shortfinned, Anguilla australis Gray, and longfinned, A. dieffenbachii, eels in two small New Zealand streams. Movements of eels commenced at dusk, with a higher proportion of shortfinned eels moving per night than longfinned eels, and also moving greater distances. Both species often showed extensive movements immediately after tagging, but thereafter movements were limited. In the smaller stream, home ranges averaged 30 and 10m for shortfinned and longfinned eels, respectively, but not all eels were active on every night. There were no seasonal differences in mean distances moved. In both streams, eel movement was almost exclusively bankside, and seldom cross-channel; eels also showed considerable fidelity to a particular bank. Shortfinned eels were most commonly found in runs, and longfinned eels in riffles.     

Cl- -HCO3- dependent ATPase in gills of freshwater and seawater adapted eels (Anguilla anguilla L.)

The gills of both seawater and freshwater adapted eels have an ATPase activity which is stimulated by anions in the presence of Mg2+. Plasma membranes were distinguished from mitochondrial membranes with specific enzyme markers, the membrane fractions separated on a discontinuous sucrose gradient, and the ATPase activity of the plasma membranes studied. Activation by the anions of Cl- or HCO3- followed Michaelis-Menten kinetics and was competitively inhibited by SCN-. The Cl- and HCO3- activation characteristics were determined: no differences between the plasma membrane ATPase activities of freshwater and seawater-adapted fishes were observed. Maximal activity measurements after solubilization of the enzymes by Triton X 100 confirmed these findings. The function of a membrane anion-dependent ATPase in the brachial epithelium of euryhaline fish is discussed.     

Redescription of Heliconema africanum (Linstow, 1899) n. comb. (Nematoda: Physalopteridae), a nematode parasite of freshwater eels (Anguilla spp.) in South Africa

The little-known nematode species Heliconema africanum (Linstow, 1899) n. comb. (Physalopteridae) is redescribed based on light and scanning electron microscopical examinations of specimens collected from the stomach of the African longfin eel Anguilla mossambica (Peters) in the Nahoon River, Eastern Cape Province, South Africa. This species, previously misidentified as Heliconema longissimum (Ortlepp, 1922), is a common parasite of eels in South Africa. The systematic status of H. longissimum, a species originally described from unidentified Australian snakes, is unclear and probably several morphologically closely related species have been included under this name.     

Development of cytochrome b primers for mitotyping of barbels (Barbus spp.)

Primers were developed that allow for rapid, reliable and inexpensive screening of cytochrome b by analysis of single-stranded conformational polymorphisms. Twenty different haplotypes were identified from six species of Iberian Barbus. These primers proved useful for population and species level studies, and could also be valuable in population genetic and phylogenetic studies of other cyprinin fishes.     

Reassessment of morphological characteristics in freshwater eels (genus Anguilla, Anguillidae) shows congruence with molecular phylogeny estimates

The morphology-based phylogeny of freshwater eels, proposed by V. Ege in 1939, has been accepted as the basis of eel classification since that time. However, this has been called into question by recent molecular studies. Most of the morphological characteristics recognized by Ege are morphometric. Since methods for the application of morphometric data to phylogeny construction have not been fully established, it is unclear whether the observed discrepancies between morphological and molecular data arise from intrinsic differences or from flawed analyses. Here, we have used two methods to assemble evolutionary trees from distance matrices constructed according to Ege's data, the neighbor-joining (NJ) method and the minimum network (MinNet) method; the latter is based on an evolutionary algorithm. After reanalysing Ege's morphological data, we found that both methods gave results consistent with those based on molecular data, although not with Ege's original classification. Therefore, we speculate that some morphological features Ege used to subdivide the eel groups may not be synapomorphic as he proposed, but symplesiomorphic or convergent . The method developed here may prove useful for constructing phylogeny for taxon groups where only continuous morphometric characteristics are recognized, such as the freshwater eels.     

Physiological responses to acute temperature increase in European eels Anguilla anguilla infected with Anguillicola crassus

The swimbladder parasite, Anguillicola crassus has infected, and spread rapidly, through European eel Anguilla anguilla (L.) populations over the past 20 to 25 yr. Our aim in the present studies was to elucidate whether the presence of A. crassus in these eels alters their rapid physiological responses to an acute temperature increase, compared to the response of uninfected fish. Both infected and uninfected fish showed significant increases in plasma cortisol after 2 h at a raised environmental temperature with increased plasma glucose after 6 h. However, infected eels exhibited a slight lag in glucose mobilisation, which may be due to the metabolic cost of harbouring a sanguiverous parasite. Both infected and uninfected fish showed a significant increase in haematocrit after 6 h of temperature elevation, but only uninfected fish exhibited a significant increase in haemoglobin at this point. However, there were no significant changes in mean erythrocyte haemoglobin concentration in either group. Our results suggest that acute temperature increase alone is unlikely to cause significant mortality of A. crassus-infected European eels; however, the effects of chronic increases in temperature in combination with other factors such as toxicants and hypoxia requires examination.     

Effects of various hormones on the sexual maturity of European eel (Anguilla anguilla L.) females from farm and lakes

Previously described and alternative methods of the induction of sexual maturation in the European eel were investigated. Weekly administrations of a gonadoliberin agonist (nnRH-A=D-Phe6-GnRH-Ea) did not induce statistically significant effect on the gonads of treated eels in none of the dosages used (0.1 microg and 10 microg/fish). Carp pituitary extract and carp pituitary extract together with a dopamine antagonist caused considerable external changes (increase in eye size) and significant gonadal development in two treatment groups: wild and cultivated stocks. The induction of the ovulation by double amount of CP and gonadoliberin agonist with dopamine antagonist mixture was not successful in a wild stock. Fertilisation of stripped eggs of farm eel was attempted unsuccessfully in, due to low egg quality. An advanced phase of the sexual maturation process could be induced in specimen infected by Anguillicola crassus indicating, that nematode infection is not a limiting factor in the artificial propagation of the European eel.     

Induced oogenesis of the European eel (Anguilla anguilla L.) in freshwater condition

European eel is a catadromous fish species, which means that after living in freshwater premature individuals adapt to sea water, and migrate to the Sargasso Sea for spawning. Although male eel can be sexually matured even in freshwater, to date, it was believed that female eel can be matured only in seawater. Here we show that the process of sexual maturation may be induced in freshwater by treating female eels with carp pituitary (GSI = 9.87 ± 1.55%). It is thus proposed that seawater condition is not an obligatory environment for stimulating gametogenesis and for artificial maturation of the European eel in neither gender.     

A comparison of highly unsaturated fatty acid levels in wild and farmed eels (Anguilla anguilla).

1. Absolute and relative amounts of eicosapentaneoic acid (EPA) and docohexaenoic acid (DHA) in muscle of eels from four different fish farms were compared with samples from wild eels from two different areas of northern Italy. 2. Farmed eels were richer in DHA and EPA than wild animals. 3. The addition of cod liver oil to the diet of farmed eels led to a significant accumulation of EPA and DHA, but no change in total lipid content. 4. The calculation of two indices related to highly unsaturated fatty acid (HUFA) content (FLQ = fish lipid quality; AI = aterogenic index), indicated the higher nutritional value of farmed vs wild fish. 5. We conclude that farmed eels are an adequate source of fish products for human nutrition and propose use of the above-mentioned indices as an effective means for assessing fish nutritional quality for populations at high risk of chronic degenerative disease.     

Changes in body musculature with sexual maturation in the European eel, Anguilla anguilla (L.)

The structure and distribution of red and white muscles have been investigated in female Anguilla anguilla of varying sexual maturity. Red muscle volumes increased with sexual maturation from approximately 5% of total muscle volume in sexually immature eels to a maximum of 13.3% in sexually maturing animals. Volume increase was due to increasing fibre diameter rather than recruitment of new fibres. Intracellular volume fractions of lipid and mitochondria increased markedly in maturing fish. Artificially matured cels showed the largest increases in muscle lipid. The possible functional roles of red and white muscle during migration are discussed.     

Changes in the gene expression profiles of the brains of male European eels (Anguilla anguilla) during sexual maturation

Background

The vertebrate brain plays a critical role in the regulation of sexual maturation and reproduction by integrating environmental information with developmental and endocrine status. The European eel Anguilla anguilla is an important species in which to better understand the neuroendocrine factors that control reproduction because it is an endangered species, has a complex life cycle that includes two extreme long distance migrations with both freshwater and seawater stages and because it occupies a key position within the teleost phylogeny. At present, mature eels have never been caught in the wild and little is known about most aspects of reproduction in A. anguilla. The goal of this study was to identify genes that may be involved in sexual maturation in experimentally matured eels. For this, we used microarrays to compare the gene expression profiles of sexually mature to immature males.

Results

Using a false discovery rate of 0.05, a total of 1,497 differentially expressed genes were identified. Of this set, 991 were expressed at higher levels in brains (forebrain and midbrain) of mature males while 506 were expressed at lower levels relative to brains of immature males. The set of up-regulated genes includes genes involved in neuroendocrine processes, cell-cell signaling, neurogenesis and development. Interestingly, while genes involved in immune system function were down-regulated in the brains of mature males, changes in the expression levels of several receptors and channels were observed suggesting that some rewiring is occurring in the brain at sexual maturity.

Conclusions

This study shows that the brains of eels undergo major changes at the molecular level at sexual maturity that may include re-organization at the cellular level. Here, we have defined a set of genes that help to understand the molecular mechanisms controlling reproduction in eels. Some of these genes have previously described functions while many others have roles that have yet to be characterized in a reproductive context. Since most of the genes examined here have orthologs in other vertebrates, the results of this study will contribute to the body of knowledge concerning reproduction in vertebrates as well as to an improved understanding of eel biology.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-799) contains supplementary material, which is available to authorized users.     

Osmoregulation in North American eels (Anguilla rostrata LeSueur) on land and in freshwater: effects of the corpuscles of Stannius

Hypercalcemia, hypomagnesia and hypophosphatemia were observed in freshwater (FW) eels (Anguilla rostrata LeSueur) after removal of the corpuscles of Stannius. These changes did not occur if Stanniectomized (CSX) eels were removed from FW and placed on land for 12 days but did occur after the eels were returned to FW. Therefore, changes in plasma electrolyte concentrations after CSX depended upon the branchial and/or integumental influx of ions. Plasma Na⁺, Cl⁻ and osmolal concentrations decreased gradually in both sham-operated (SHM) and CSX eels on land (12 days) and in FW (12 days). Plasma K⁺almost doubled in both SHM and CSX eels after 4 days on land, remained elevated, and fell abruptly to normal within a day after the eels were returned in FW. After 2 days on land, urine flow rates in SHM and CSX eels had decreased by approximately 85%, osmolar clearance by 50% and positive free-water clearance by more than 90%. Body weights did not decrease when eels were on land so it was concluded that the reduced but continuous renal loss of water was counterbalanced by the integumental uptake of condensed water. Accepted: 21 October 1998     

Changes in the skin-scale complex with sexual maturation in the European eel, Anguilla anguilla (L.)

Structural features of the epidermis, dermis and scales were examined in adult female Anguilla anguilla of varying sexual maturity. Advanced sexual stages were obtained by hormone injection. The dermis increased in thickness with both size and sexual development. Epidermal thickness was unrelated to size or maturity but mucous cell densities decreased in more mature animals. Hormone treated eels showed a loss of mucous cells accompanied by degeneration of the epidermis. Scale areas increased from 50% in sexually immature adults to 145% in sexually maturing eels. Skin calcium values ranged from 0.27 to 0.83 mg cm⁻² and did not show any relation to either scale or sexual maturity. The possible relevance of structural changes to migration is discussed.     

Surgical implantation of radio tags in three eel species (Anguilla spp.) in South Africa

Studies have reported poor survival of surgically tagged freshwater fishes in warm African waters. This study aimed to assess the applicability of using radio telemetry (and surgical implantation of tags) for Anguilla spp. Nineteen yellow eels (Anguilla bengalensis, A. marmorata and A. mossambica) were surgically implanted with radio tags between October 2018 and January 2019 in the Thukela River, South Africa. Most eels were alive 6 months after tagging, and recaptured eels displayed advanced or complete healing at the incision site. Therefore, this method appears suitable for African freshwater eels.     

Changes of iron content in eels (Anguilla japonica) infected with atypical Aeromonas salmonicida

1. Hb, MCHC, Na, Ca, Mg and Cu in plasma decreased with atypical Aeromonas salmonicida infection. Whilst plasma K and NPN increased.2. Plasma Fe decreased markedly with infection. No statistically significant change in UIBC was found, though moribund eels showed slightly lower values compared to that of the control. The rate of decrease in TIBC is similar to that in most elements in plasma.3. Fe content in most tissues decreased with infection. It increased in the gills and head muscle (infection site). No significant change was found in the intestine.4. Water content in various tissues increased with infection.