Lack of species-specific primer effects of odours from female Atlantic salmon, Salmo salar, and brown trout, Salmo trutta

We exposed, in two successive spawning seasons, individually placed precocious male Atlantic salmon ( Salmo salar ) and brown trout ( Salmo trutta ) parr to odour stimuli (ovarian fluid and urine mix) from ovulated conspecific or heterospecific anadromous females. Atlantic salmon parr had significantly higher plasma concentrations of the hormones 17α,20β-dihydroxy-4-pregnen-3-one (17,20β-P), 11-ketotestosterone (11-KT) and testosterone (T) after exposure to odours from conspecific females or from brown trout females compared to parr exposed to a control solution (0.9% NaCl). We did not observe any significant differences between the hormone levels in salmon parr exposed to the two female odours. The salmon parr exposed to conspecific odours had significantly higher volumes of strippable milt compared to the controls, but we did not find any significant differences when comparing the effect of the two female odours. Brown trout parr had significantly higher plasma 17,20β-P levels following exposure to heterospecific female odours compared to control males, but there was no significant difference between males exposed to the different female odours. We did not observe any significant differences in plasma levels of T and 11-KT and in milt volumes between exposed and control trout. Taken together, the results from both tested species indicate that the potency of heterospecific stimuli in stimulating increased plasma sex steroid hormone levels in male parr was as strong as stimuli from conspecific females. The results are discussed in connection to observed hybridisation between the two sympatric species.     

Sublethal effects of the pesticide Diazinon on olfactory function in mature male Atlantic salmon parr

Diazinon, an organophosphate pesticide, had a sublethal effect on the olfactory system of mature male Atlantic salmon parr. The olfactory responses of the parr to prostaglandin F_2a (PGF_2a) were studied after exposure of the epithelium to different concentrations of Diazinon in water. Electrophysiological recordings from the epithelium indicated that the responses to this prostaglandin were significantly reduced at nominal concentrations as low as 1.0μg l⁻¹ and the threshold of detection was reduced 10-fold at 2.0 μg 1⁻¹ . Mature male salmon parr exposed for a period of 120 h to Diazinon (nominal concentrations 0.3, 0.8, 1.7, 2.7, 5.6, 13, 28 and 45 μg 1 ⁻¹) also had significantly reduced levels of the reproductive steroids, 17,20β-dihydroxy-4-pregnen-3-one, testosterone and gonadotrophin II in the blood plasma after priming with ovulated female salmon urine. Both prostaglandin F_2a and ovulated female urine are known to have important roles in synchronizing reproductive physiology and behaviour in salmonids as well as other fish species. The results are therefore discussed in relation to the possible sublethal effects of Diazinon on reproduction in the Atlantic salmon and possible effects on populations of salmonids.     

An electrophysiological study on the effects of pH on olfaction in mature male Atlantic salmon (Salmo salar) parr

The olfactory responses of mature male Atlantic salmon ( Salmo salar L.) parr to known odorants were studied after exposure of the olfactory epithelia to water of varying pH. Electrophysiological recordings from the olfactory epithelia indicated that the responses of fish to both testosterone and urine from ovulated female Atlantic salmon were significantly reduced at pH 5·5 and 4·5 and abolished at pH 3·5. Concentration response studies indicated that at pH 5·5 and 6·5 significantly higher concentrations of testosterone and urine were required to produce the same amplitude responses as controls. Both testosterone and urine have previously been shown to be important chemical cues eliciting behavioural and physiological responses in Atlantic salmon. The results are therefore discussed in relation to the possible sublethal effects of acidification on reproduction and behaviour of Atlantic salmon and the effects on salmonid stocks.     

The role of F-series prostaglandins as reproductive priming pheromones in the brown trout

Electrophysiological studies demonstrated that the olfactory epithelium of mature male brown trout Salmo trutta parr was acutely sensitive to F-series prostaglandins (PGFs) PGF_1α and PGF_2α, with detection threshold concentrations of 10⁻¹¹ M. The olfactory epithelium was also sensitive to the PGF metabolite 15-ketoPGF_2α (threshold 10⁻⁸ m), but did not detect a further metabolite, 13,14,-dihydro-15-ketoPGF_2α Immature brown trout did not detect any of the prostaglandins tested. Exposure of mature male brown trout parr to waterborne PGF_1α and PGF_2α (concentration 10⁻⁸ m), resulted in significant increases in levels of expressible milt and the plasma concentrations of 17,20β-dihydroxy-4-pregnen-3-one, testosterone and 11-ketotestosterone. The olfactory epithelium of both immature and mature male brown trout parr was sensitive to the urine and ovarian fluid from ovulated female brown trout. Exposure of mature male brown trout parr to ovarian fluid resulted in an increase in the levels of plasma 17,20β-dihydroxy-4-pregnen-3-one whilst exposure to urine increased the levels of expressible milt. In addition, PGF_2α was found to be present within both the urine and ovarian fluid of mature female brown trout. It is suggested that the F-series prostaglandins have a role as priming pheromones in male brown trout.     

Reproductive priming in mature male Atlantic salmon parr exposed to the sound of redd cutting

The sounds of a wild female Atlantic salmon cutting a redd were associated with significant increases in the levels of plasma 17,20β-dihydroxy-4-pregnen-3-one (17,20βP) and of expressible milt in mature male parr, comparable with levels of the steroid and milt produced in parr exposed to the priming pheromone, prostaglandin F_2a. Hence auditory cues may have a significant role in synchronising reproductive physiology in Atlantic salmon.     

The impact of two pesticides on olfactory-mediated endocrine function in mature male Atlantic salmon (Salmo salar L.) parr

Short-term exposure of the olfactory epithelium of mature male Atlantic salmon parr to either the pesticide simazine (concentrations 1.0 and 2.0 microg l(-1)) or the pesticide atrazine (concentration 1.0 microg l(-1)) significantly reduced the olfactory response to the female priming pheromone, prostaglandin F(2alpha). In addition, the reproductive priming effect of the pheromone on the levels of expressible milt was also reduced after exposure to the individual pesticides (simazine 0.1, 0.5, 1.0 and 2.0 microg l(-1) and atrazine 0.5 and 2.0 microg l(-1)). When the olfactory epithelium was exposed to a mixture of simazine and atrazine, (concentrations of 0.5:0.5 and 1.0:1.0 microg l(-1)), there was no significant reduction in the olfactory response when compared to the single pesticides at equivalent concentrations. In addition, exposure to a mixture of simazine and atrazine had no synergistic effect on the priming response, and plasma levels of testosterone, 11-ketotestosterone and 17,20beta-dihydroxy-4-pregnen-3-one were similar in the groups of male parr exposed to the individual pesticides. Although the levels of expressible milt were reduced in all groups, there were no significant differences between the different pesticide treatments. The results of the study suggest that the two s-triazine pesticides have an additive and not a synergistic impact on olfactory-mediated endocrine function in mature male salmon parr.     

Dynamics of excretion of 17α,20β-dihydroxy-4-pregnen-3-one 20-sulphate, and of the glucuronides of testosterone and 17β-oestradiol, by urine of reproductively mature male and female rainbow trout (Oncorhynchus myklss)

Levels of sulphated 17α20β-dihydroxy-4-pregnen-3-one (17,20 β -P; the oocyte maturation inducing steroid) in blood plasmas of sexually mature male and female rainbow trout Oncorhynchus mykiss , were very low in comparison to those of the free steroid. However, relatively large amounts were found in urine of both sexes.
Catheters were inserted into the urinary bladders of unovulated and ovulated females and of ripe-running males, and the fish then placed in spawning channels. Three-hourly urine samples were collected between 09.00 and 18.00 hours and then a 15-h sample between 18.00 and 09.00 hours the next morning. Measurements were made of 17,20 β -P-sulphale, testosterone glucuronide (T-G) and 17 β -oestradiol glucuronide (E2-G). In females, the highest rates of excretion of E2-G, T-G and 17,20 β -P-sulphate were found in unovulated, ovulating and ovulated females, respectively. The rates of excretion of 17,20 β -P-sulphate, T-G and E2-G in ovulated females were unaffected by the presence of a male. id males, however, there was a sharp increase in the rate of excretion of 17,20 β -P-suiphate and T-G in fish which were paired with an ovutated (nesting) female. A similar increase was found in males injected with male trout pituitary extract.     

The involvement of gonadotrophin and sex steroids in the control of reproduction in the parr and adults of Atlantic salmon, Salmo salar L.

Early sexual maturity occurred in the majority of male Atlantic salmon parr. Levels of the plasma androgens testosterone and 11-ketotestosterone rose steadily as the male parr matured, and decreased as the testes regressed. No such progressive changes were observed in the plasma gonadotrophin (GTH) levels, although the pituitary GTH levels were much higher in mature than in immature male parr; reasons for this, incluiding the possibility that the GTH radioimmunoassay employed is inadequate, are discussed. All female parr remained immature throughout the year, although the gonadosomatic index did show an annual cycle. Adult salmon had higher GTH and sex steroid levels than parr at the same stage of sexual maturity, the levels corresponding to the degree of sexual development of the adult fish.     

Urine of ovulated female masu salmon attracts immature male parr treated with methyltestosterone

Methyltestosterone-treated immature male masu salmon Oncorhynchus masou parr were attracted to both the urine of ovulated females and the ether soluble basic substances extracted from the urine, but not to immature female urine. It is suggested that the male response to the sex attractant (releaser pheromone) in the urine is under the control of androgens.     

Allozyme heterozygosity, date of first feeding and life history strategy in Atlantic salmon

The relations between allozyme heterozygosity, relative date of first feeding and life history strategy in juvenile Atlantic salmon Salmo salar were examined using eggs obtained from a 400 family cross (20 male × 20 female adult Atlantic salmon). Multilocus heterozygosity, through its positive associations with the timing of first feeding and growth rate, was correlated with life history strategy in juvenile Atlantic salmon, albeit under genotype × environmental (temperature, food availability) regulation. Under hatchery conditions, a 10 day difference was observed in the relative date of first feeding between early and late first feeding Atlantic salmon. Early first feeding Atlantic salmon exhibited a significantly higher mean heterozygosity, grew faster at ambient water temperature (April to November) and a significantly higher proportion adopted the early freshwater maturation (age 0+ years, male fish) or early migrant (age 1+ years, mainly female fish) strategies compared to late first feeding Atlantic salmon. Elevated water temperatures over the winter (December to April, >10·5° C) provided additional growth opportunity allowing previously mature male parr (mainly early first feeders) and lower modal group parr (mainly late first feeders) to adopt the early migrant strategy by the following spring.     

Does the Refuge Availability Influence the Spawning Behavior of Mature Male Parr in Salmonids? A Test in the Miyabe Charr

In many salmon and charr, both 'migratory males' and 'precocious males' are maintained as alternative life-histories within a population. During breeding, precocious males gather around the mating pair of migratory fish and attempt to sneak in the spawning between larger male and female charr. Refuges such as debris and shallow areas may provide shelter from aggressive attacks and allow precocious males to hold positions closer to the pair (nest) and/or sneak more easily during the mating. Here we examine whether the availability of refuges influences the breeding behavior of precocious male parr of the Miyabe charr under experimental and natural conditions. Aggressive attacks directed toward precocious parr by the mating pair or other parr was not influenced by the refuge availability either under experimental conditions or in the wild. We did not find the effect of high refuge availability on the proximity of parr to the nest beyond the experimental conditions where the density of refuges was probably higher than in the natural stream. There were no effects of high refuge availability either on parr's attempts at sneak mating or on their success in spawning. Thus, our results provide little evidence that the refuge availability influences parr sneaking behavior. Other possible effects of high refuge availability, for example, the increase of fertilization success and the decrease of energy expenditure and risk taking, remain to be considered.     

A method for tracking the behaviour of mature and immature salmon parr around nests during spawning

A remote monitoring system was developed to provide information on the behaviour of mature and immature Atlantic salmon Salmo salar parr at nests during the spawning season. An octagonal passive integrated transponder (PIT) detector (0·865 m maximum diameter) designed to surround nests of Atlantic salmon was used to identify individual salmon parr present at 38 spawning events in three circular spawning channels. The range of the detector for PIT tags presented in the optimum orientation was 2·4 cm (range between tags 1·7–3·0 cm). Using a sub-sample of 20 spawnings, the mean efficiency of the detector (number of fish passes registered relative to number of passes observed on video) was 70·5% (range 32-100%). There were no significant effects of time from spawning, total number of registrations, body size or maturity status (mature or immature) on efficiency. However, fish were more likely to be detected entering nests than leaving, as departures were more rapid and higher in the water column. The PIT detector did not affect the numbers of parr at spawnings or between spawning intervals of females, and allowed for the individual identification of 65 of the 72 parr observed in nests during spawning. In all cases where certain identifications were not possible and the video was of satisfactory quality, this was due to obstruction of the camera view by anadromous fish. The remote monitoring system was thus effective in identifying behavioural differences, and only one of 20 immature parr was ever detected during the period encompassing 10 min before and after spawning compared with 30 or 40 mature parr.     

The downstream migration of precociously mature Atlantic salmon, Salmo salar L, parr in autumn; its relation to the spawning migration of mature adult fish

The autumn emigration of juvenile Atlantic salmon, Sulmo salur L. from the Girnock Burn, Aberdeenshire, is shown to be comprised of two components. Precociously mature males and sexually immature fish differ in their dependence on seasonal and biological cues for the release of migratory behaviour. The emigration of ripe mature male parr is shown to follow the entry of mature adult salmon to the stream; when adult fish are prevented from entering the stream, the emigration is induced by seasonal factors. Spent male parr tend not to participate in the autumn emigration. The emigration is considered to be principally an appetitive phenomenon which maximizes the number of precociously mature males attaining sexual contact with adults.     

The Gonadotropic Cell in Parr,Precocious Parr Male and Smolt of the Atlantic Salmon,Salmo salar. An Immunocytological,Light- and Electron Microscopical Study

Lindahl, K. 1980. The gonadotropic cell in parr, precocious parr male and smolt of the Atlantic salmon, Salmo salar. An immunocytological, light- and electron microscopical study. (Department of Zoology, University of Stockholm, Sweden.) — Acta zool. (Stockh.) 61(2): 117–125. Only one GTH cell type was identified in the pars distalis of the parr, smolt and precocious parr male. On a fine structural basis four phases with transitional forms of the GTH cell were recognized. In parr and smolt the GTH cells have numerous secretory granules and their cytology substantiate that they are in a storing phase with a possibly low release rate. On the contrary, in the precocious parr male all phases of the GTH cell are present. The great number of active cells and frequent degranulation and vacuolization indicate a high activity and release level.     

Relative ventricular weight of wild Atlantic salmon parr in relation to sex, gonad maturation and migratory activity

Relative ventricular weight (RVW, ventricular weight/body weight · 100) was measured for five groups of Atlantic salmon parr from the Girnock Burn in Scotland. The mean RVW was: mature males, 0.087; immature resident males, 0.054; immature resident females, 0.056; immature migrant males, 0.056; immature migrant females, 0.053. For a group of mature male parr from the R. Nith, Galloway, Scotland, the mean RVW was 0.108. There were no significant differences in the RVW between groups of immature fish. The RVW of each group of mature male parr was significantly greater than those of each, group of immature parr. Condition indices (weight/length³) were closely similar between all groups of parr. The functional significance of plasticity in ventricular weight is discussed in relation to life histories of Atlantic salmon.     

Timing of first feeding and life-history strategies in salmon: genetic data

To investigate the relationship between genetic composition and some physiological traits of interest (age at smoltification, precocious maturation in male parr) in early and late first feeding Atlantic salmon, genetic variation at 6 isozyme and 8 microsatellite loci was examined. Early and late first feeding salmon showed different allelic and genotypic distributions at both isozyme and microsatellite loci. A positive relation between enzymatic loci heterozygosity and precocious active alimentation and earlier smoltification (S1 cf. S2) were also found.     

Stimulatory and inhibitory effects of testosterone on testes in Atlantic salmon male parr

Immature 1-year-old Atlantic salmon Salmo salar parr were implanted with Silastic capsules of different sizes filled with testosterone (T). Testosterone had both positive and negative effects on testicular weights, spermatogenesis and steroidogenesis. The positive effects: higher incidence of males with enlarged gonads, spermiation, and high plasma levels of 11-ketotestosterone (11-KT) and 17,20β-dihydroxy-4-pregnen-3-one (17,20β-P), were most pronounced in males treated with small T capsules. The negative effects: suppression of gonadal development and depressed plasma levels of 11-KT and 17,20β-P compared with mature controls, were most evident in fish treated with large T capsules.     

Differential expression of Atlantic salmon thyrotropin β subunit mRNA and its cDNA sequence

To study the regulation of the thyroid system, an Atlantic salmon Salmo salar cDNA clone was isolated for thyroid stimulating hormone (TSH) β subunit gene. A cDNA (866 bp) was isolated from an adult Atlantic salmon pituitary cDNA library, this clone was sequenced and shown to be highly conserved when compared to other teleost β TSH subunit sequences. The cDNA was used as a probe for Northern blot analysis of total pituitary RNA from the different life cycle stages of Atlantic salmon. Northern blot analysis demonstrated that β TSH mRNA is expressed at all life cycle stages studied, including parr, smolt, immature fish at sea and sexually mature male fish. Densitometry of Northern blots showed that sexually mature male salmon had low levels of salmon β TSH mRNA compared to non-mature fish. Stunts, fish performing poorly in salt water, were shown to have elevated levels of β TSH mRNA when compared to healthy fish.     

Seasonal changes in androgen levels in stream- and hatchery-reared Atlantic salmon parr and their relationship to smolting

In stream-reared Atlantic salmon Salmo salar , plasma androgens were significantly greater in mature male parr than immature males and females in October, but had declined by January and did not differ significantly from immature fish throughout the spring. Immature fish in March were significantly larger and had greater gill Na⁺, K⁺-ATPase activity than their previously mature counterparts. Bimodal growth distribution was seen in hatchery-reared Atlantic salmon and a proportion of the male fish in the lower mode matured. Plasma testosterone (T) and 11-ketotestosterone (11-KT) were significantly elevated from September to December in mature male (1+ year) parr. In January, plasma androgens had declined in mature males and did not differ significantly from immature fish. By May all the hatchery fish were large enough to smolt and a proportion of the previously mature males had increased gill Na⁺, K⁺-ATPase activity. Therefore elevated androgens in the previous autumn do not prevent smolting. Parr with higher plasma T and 11-KT in April and May, that are presumably beginning to mature, had lower gill Na⁺, K⁺-ATPase activity, indicating that future maturation and associated increases in androgens may inhibit smolting.     

The effects of intraperitoneally implanted dummy acoustic transmitters on the behaviour and physiology of juvenile Atlantic salmon, Salmo salar L

The behavioural and physiological effects of surgical implantation of dummy miniature acoustic transmitters into the peritonealcavities ofjuvenile Atlantic salmon, Salmo salar L., were assessed. lntraperitoneal implantations had no significant effect on growth, feeding or swimming behaviour in either parr or smolts. Recovery from the surgical implantation was both rapid and total; infection was absent; and physiological processes such as smoltification and maturation of testes in precocious parr were unaffected. Expulsion of the transmitter through the body wall, not through the implantation wound, occurred in a number of fish but without adversely affecting the animals. The intraperitoneal implantation technique is discussed in relation to its use during biotelemetry studies.