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- Olfactory sensitivity to conspecific bile fluid and skin mucus in the European eel Anguilla anguilla (L.)Publication . Huertas, Mar; Hubbard, Peter; Canario, Adelino V. M.; Cerda, J.The present study assessed the olfactory potency of conspecific bile fluid and skin mucus in the European eel Anguilla anguilla by the electro-olfactogram. Immature males showed high olfactory sensitivity to conspecific bile, giving large amplitude responses in a concentrationdependent manner with estimated thresholds of detection of <1:107 (n = 6). Mucus also proved to contain highly potent odorants with thresholds of detection of c. 1:106 (n = 6). Crude solidphase extraction of bile fluid (C-18 and C-2/ENV+ cartridges) showed that the majority of olfactory activity in bile fluid was contained in the eluate of C-18 cartridges (n = 6). There were quantitative differences, however, between the sexes; female bile fluid had a higher proportion of activity in this fraction. Similar solid-phase extraction of mucus showed that it contains a higher proportion of odorants in the C-18 filtrate than bile fluid. Mucus from mature eels, however, had a higher proportion of olfactory activity in the eluate than immature fish (n = 6). Cross-adaptation experiments suggest that there are qualitative differences in the odorants contained in bile and mucus depending on both the sex and state of sexual maturation of the donor (n = 6). These results are consistent with a role for chemical communication in the reproduction of the European eel and suggest that both bile and mucus are potential sources of the odorants involved.
- Follow your nose: chemical communication throughout the European eel (Anguilla anguilla, L.) life-cyclePublication . Huertas, Mar; Canario, Adelino V. M.; Hubbard, PeterEuropean eels are important in both scientific and economic terms. Unfortunately, current populations are becoming increasingly endangered and urgentmanagement is needed. Several aspects of eel biology, together with their highly developed sense of smell, suggest that chemical communication could be involved at key stages of their life-history. Thus, advances in this area could generate novel tools for stock management.
- Changes in the gene expression profiles of the brains of male European eels (Anguilla anguilla) during sexual maturationPublication . Churcher, Allison; Pujolar, Jose M.; Milan, Massimo; Hubbard, Peter; Martins, Rute S. T.; L. Saraiva, João; Huertas, Mar; Bargelloni, Luca; Patarnello, T.; Marino, Ilaria A. M.; Zane, Lorenzo; Canario, Adelino V. M.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.
- Changes in olfactory sensitivity during the European eel (Anguilla Anguilla) life cyclePublication . Huertas, Mar; Canario, Adelino V. M.; Hubbard, PeterThe aim of this study was to test whether physiological changes are paralleled by changes in olfactory function during different stages of the European eel’s life-cycle. Sensitivity to diverse odorants (amino acids, bile acids, bile fluids, Na+ and Ca2+) was assessed by extra-cellular recording from the olfactory nerve of seawater or freshwater and immature or mature males. Sensitivity to amino acids did not differ markedly, whether fresh- or seawater-adapted, immature or mature. Sensitivity to bile acids and bile fluid, however, depended on the physiological status; in general, freshwater eels were more sensitive to bile acids than seawater fish.
- Olfactory sensitivity to bile fluid and bile salts in the European eel (Anguilla anguilla), goldfish (Carassius auratus) and Mozambique tilapia (Oreochromis mossambicus) suggests a 'broad range' sensitivity not confined to those produced by conspecifics alonePublication . Huertas, Mar; Hagey, L.; Hofmann, A. F.; Cerda, J.; Canario, Adelino V. M.; Hubbard, PeterTeleosts have high olfactory sensitivity to bile salts. To assess whether this phenomenon is involved in intra-specific chemical communication alone, or is part of a more ‘broad range’ sensitivity to bile salts produced by heterospecifics, we investigated possible differences in the odour of bile between the sexes and among different species – the eel (Anguilla anguilla), goldfish (Carassius auratus) and Mozambique tilapia (Oreochromis mossambicus) – using the electro-olfactogram (EOG). We also identified the main bile constituents by liquid chromatography and mass spectrometry. There were marked differences in olfactory response of the eel to thin-layer chromatography fractions of bile from both sexes, and mature and immature conspecifics. Smaller differences were seen in the potency of fractions of bile from male and female goldfish and tilapia. Eels, goldfish and tilapia demonstrated similar olfactory sensitivity to bile from a range of different species, with no apparent correlation between the olfactory potency of bile and a phylogenetic closeness and/or similarity of diet of the donor to the receiver. The three species were able to detect odorants in thin-layer chromatography fractions of heterospecific bile even in the absence of activity in conspecific bile. Eels, goldfish and tilapia responded to both sulphated C27 bile salts (5-scymnol-sulphate and 5-cyprinol sulphate) and to taurine-conjugated C24 bile salts (taurochenodeoxycholic acid, taurolithocholic acid and taurocholic acid), irrespective of whether these bile salts were present in conspecific bile. Together, these results suggest that teleosts have a broad-range olfactory sensitivity to bile salts, with potential roles in both intra-specific chemical communication and in inter-specific interactions.
- Sexually mature European eels (Anguilla anguilla L.) stimulate gonadal development of neighbouring males: possible involvement of chemical communicationPublication . Huertas, Mar; Scott, A. P.; Hubbard, Peter; Canario, Adelino V. M.; Cerda, J.This study was aimed to investigate whether sexual maturation of immature male eels could be stimulated indirectly by placing them in contact with either male (Minj) or female (Finj) eels in which sexual maturation had been stimulated directly by weekly injections of human chorionic gonadotropin (hCG) or salmon pituitary extract (SPE), respectively. Untreated males were placed either in the same tank or in a separate tank that was linked to the injected Wsh via a recirculation system. The hormonal treatments stimulated spermatogenesis and spermiation in Minj, and ovulation in Finj as well as an increase of the ocular (Io) and gonadosomatic (GSI) indices in both sexes. Plasma levels of testosterone (T) and 11-ketotestosterone (11-KT) increased in Minj and T and 17 -estradiol (E2) in Finj. A small peak of plasma 17,20 -dihydroxypregn-4-en-3-one (17,20 P) occurred during ovulation, while the plasma levels of 17 -hydroxypregn-4- ene-3,20-dione (17P) were undetectable in both males and females. The water conditioned by Minj and Finj induced signiWcant, though relatively minor, increases in Io and GSI in uninjected males. In addition, uninjected Wsh showed small changes in plasma T and 11-KT levels, apparently related to the timing of spermiation and ovulation of Minj and Finj, respectively, as well as an activation of spermatogenesis (but not spermiation). Injected Wsh released free and conjugated T, 11-KT and E2 into the water, although immature eels were unable to smell (by electro-olfactogram) any of these steroids or prostaglandin F2 . However, immature males were highly sensitive to water extracts conditioned by spermiating Minj and pre-ovulatory and ovulated Finj. These preliminary results suggest the existence of chemical communication between maturing eels and immature males that stimulates gonad development, although the putative pheromone(s) involved has/have not yet been identiWed.
- Evidence for involvement of chemical communication in reproduction of the eel Anguilla anguillaPublication . Huertas, Mar; Hubbard, Peter; Scott, A. P.; Canario, Adelino V. M.; Cerda, J.The European eel (Anguilla anguilla) is characterised by long transoceanic migration to spawning sites during which the fish become sexually mature. A previous study demonstrated that mature eels may induce physiological and behavioural changes in immature conspecifics. This raises the possibility that chemical communication may be involved in this process. The aim of the current study was, therefore, to assess the olfactory sensitivity of eels to conspecific-derived odours and to establish whether these odours differ according to sex and/or state of maturity.
- Chemical communication in the Genus Anguilla: a minireviewPublication . Hubbard, Peter; Canario, Adelino V. M.; Huertas, MarEels of the Genus Anguilla are important fish in both scientific and economic terms. Unfortunately, current stocks of the European eel in particular (Anguilla anguilla L.) are becoming increasingly endangered. Chemical communication plays important roles in several key aspects of fish biology. Due to its complex life-cycle, the eel offers a unique opportunity to study various aspects of olfactory biology and chemical communication almost in isolation, feeding (during freshwater ‘yellow’ stage), adaptation to seawater, migration and, finally, reproduction. The aim of this brief review is to summarise what is known about chemical communication in the eel (during reproduction in particular) and, more importantly, stimulate further research. To date, eels have been shown to have high olfactory sensitivity to substances released by conspecifics. Both the bile fluid and skin mucus have been implicated as the routes of release of these odorants but other routes, such as the urine, cannot be excluded. Furthermore, the nature of these odorants depends on both the sex and reproductive status of the donor; exposure to water conditioned by mature con-specifics causes a stimulation of sexual maturation in immature eels. These results are consistent with a role for chemical communication in eel reproduction. The European eel is, therefore, proposed as a model species for studies on olfaction and chemical communication in fish because of its ancestral status, its high olfactory sensitivity and its physiological plasticity. However, more research is necessary; specifically, identification of the key odorants involved, their behavioural and physiological effects and how the olfactory system may change at various stages of its life-cycle.
- Tilapia male urinary pheromone stimulates female reproductive axisPublication . Huertas, Mar; Almeida, O. G.; Canario, Adelino V. M.; Hubbard, PeterMozambique tilapia males congregate in leks where they establish dominance hierarchies and attract females to spawn in sandy pits. Dominant males store more urine than subordinates and the pattern of urination and the high sensitivity of females to male urine suggest chemical signalling via the urine. Here we show that pre-ovulated and post-spawn females when exposed to dominant male urine increased significantly, in less than 1 h, the release rate of the maturation-inducing steroid 17,20bdihydroxypregn- 4-en-3-one which is maintained elevated for at least 6 h. This indicates a pheromonal role for male urine in the synchronisation of spawning. Furthermore, we show that the lack of affinity of 17,20bP to sex steroid binding globulin explains, at least partly, its rapid release and lack of detection in the blood. Thus tilapia urine involvement in several communication processes confirms that cichlids have evolved a sophisticated chemical signalling system together with their complex visual, acoustic and behavioural displays.