Paternal reproductive strategy influences metabolic capacities and muscle development of Atlantic salmon (Salmo salar L.) embryos

Male Atlantic salmon follow a conditional strategy, becoming either "combatants" that undertake a seaward migration and spend at least a year at sea or "sneakers" that remain in freshwater and mature as parr. A variety of physiological indices showed significant but small differences between the offspring of males that use these two reproductive tactics. Offspring fathered by anadromous male Atlantic salmon (Salmo salar L.) showed greater muscular development and muscle metabolic capacities but lower spontaneous movements than those fathered by mature male parr. At hatch and at maximum attainable wet weight (MAWW), offspring fathered by anadromous males had higher activities of mitochondrial (cytochrome C oxidase and citrate synthase) and glycolytic (lactate dehydrogenase [LDH]) enzymes than progeny of mature male parr. Enzymatic profiles of progeny of anadromous fathers also suggested greater nitrogen excretion capacity (glutamate dehydrogenase) and increased muscular development (creatine kinase and LDH) than in the progeny of mature parr. At MAWW, juveniles fathered by mature parr made considerably more spontaneous movements, presumably increasing their energy expenditures. For juveniles fathered by anadromous males, total cross-sectional areas of white and red muscle at hatch were higher due to the greater number of large-diameter fibers. We suggest that the slightly lower metabolic capacities and muscular development of alevins fathered by mature parr could reflect differences in energy partitioning during their dependence on vitellus. Greater spontaneous movements of offspring of mature male parr could favor feeding and growth after the resorption of the vitellus.     

Mating success of alternative maturation phenotypes in male Atlantic salmon,Salmo salar

Summary Mature male parr successfully fertilized eggs of anadromous female Atlantic salmon, Salmo salar, in competition with anadromous males under simulated natural conditions. Mating situations were created in which mature male parr and anadromous males competing for the opportunity to spawn with an anadromous female differed in allelic forms of the same enzyme. Females deposited eggs into a sequence of 3 or 4 eggs nests. The mean proportion of eggs in a redd fertilized by parr increased with increasing numbers of parr present at a redd, reaching 23% at male parr: anadromous male ratios of 20:1. Single male parr fertilized, on average, 5% of the eggs in a redd. The proportion of eggs in an egg nest fertilized by parr also depended upon the order of egg nest construction, such that parr mating success was highest at the initial nest constructed and lowest at the final nest. Parr have relatively high fertilization success for their size when compared with the smaller maturation phenotype of other salmonids.     

Epidermis thickness and secondary sexual characters in mature male and immature Baltic salmon, Salmo salar L., parr: seasonal variations and effects of castration and androgen treatment

At the breeding season (November) the mature male parr had a thicker epidermis than had the immature parr. In winter (February) there was no difference, while in May, at the smoltification period, the previously mature male parr had a thicker epidermis than the immature parr. In both categories of fish the epidermis was thinner in May than in November. The epidermal thickness in castrated male parr was the same as in immature parr. Treatment with 11-ketoandrostenedione (llkΔ4) increased epidermal thickness in castrated males. Treatment with testosterone and llkΔ4 increased epidermal thickness in previously mature males in spring. There was no development of anadromous secondary sexual characters (hooked lower jaw, adult nuptial colouration) in any male.     

Sperm quality in the alternative reproductive tactics of Atlantic salmon: the importance of the loaded raffle mechanism.

The outcome of sperm competition in species with alternative male reproductive strategies may be determined by fair or loaded raffle mechanisms. The sperm production and quality of male Atlantic salmon using alternative reproductive tactics were investigated in order to determine the relative importance of sperm quality for male reproductive success. Sexually mature resident parr males produced greater numbers of spermatozoa per millilitre of ejaculate and invested more in their gonads as a percentage of body mass than their anadromous counterparts. Parr males had greater proportions of motile spermatozoa and a greater sperm ATP content as compared with anadromous males. Parr males invested relatively more in sperm quality and sperm numbers after the effect of body size was accounted for. In fertilization experiments, parr males fertilized greater proportions of eggs than anadromous males. A polynomial model exhibited a trade-off between testes mass and ejaculate expenditure and explained 60% of the variation. These results establish that, in sperm competition with dominant males, parr males may compensate for behavioural subordinance by producing physiologically superior spermatozoa.     

Individual growth and phase differentiation of lacustrine masu salmon, Oncorhynchus masou, under artificial rearing conditions

 In lacustrine masu salmon, Oncorhynchus masou, originated from anadromous fish and inhabiting an artificial lake (Shumarinai Lake), we examined the relationship between individual growth during the juvenile stage and phase differentiation under artificial rearing conditions. In females, the mean fork length of potential (subsequent) 1+ smolts and potential 1+ parr (1+ parr show fish that neither smolted nor matured until 1+ autumn) always differed after their first summer (0+ summer), the former being larger. In males, the juveniles that grew faster during their first spring became 0+ mature male parr. After their first summer, potential 1+ smolts were always larger in body length than potential 1+ mature parr and potential 1+ parr. These results were similar to previous reports of anadromous masu salmon, suggesting that the lacustrine masu salmon studied seems to have maintained the phase differentiation as in the original fish, likely because only 60 years have passed since the formation of the lacustrine population.     

Age at maturity in landlocked and anadromous Atlantic salmon parr from two Québec rivers

Synopsis Age at maturity in male Atlantic salmon parr from landlocked populations in the Watshishou and Musquaro Rivers is significantly greater than in anadromous populations from the same rivers. We conclude that high post-smolt mortality in anadromous stocks is conducive to male parr maturity at an early age. We also suggest that the lower proportion of maturing male parr in landlocked stocks may be related to competition among males for mates and the smaller ultimate size of spawning adult landlocked salmon.     

Multiple paternity and variance in male fertilization success within Atlantic salmon Salmo salar redds in a naturally spawning population

The incidence and magnitude of multiple paternity were estimated for a natural, unmanipulated spawning population of Atlantic salmon Salmo salar. Egg nests were surveyed in the autumn and sub‐samples were excavated the following spring. Parentage data derived from microsatellite DNA revealed an unexpectedly high level of multiple paternity. Within a single redd, females may mate with as many as 16 different males, including small mature male parr and large anadromous males. Multiple paternity was most pronounced in areas of highest redd density, corresponding with increased abundances of mature male parr. In addition, there was considerable variation in success among males, although this variability did not depend upon the number of males participating in spawning. This work underscores the value of undertaking genetic studies on the mating systems of fishes in unmanipulated, natural environments.     

Patterns of Aggression and Operational Sex Ratio Within Alternative Male Phenotypes in Atlantic Salmon

The intensity of male–male aggression during mating is predicted to increase with the operational sex ratio (OSR) (the ratio of sexually active males to females). We observed aggressive behaviour in relation to OSR within alternative phenotypes (large anadromous males and small ‘sneaker’ mature male parr) of Atlantic salmon, Salmo salar, as they competed for access to anadromous females in large outdoor arenas immediately prior to spawning events as well as throughout the spawning season. Anadromous males were primarily aggressive outside of spawning events, and their aggression increased with OSR over a narrow range of 0.08–4. By contrast, mature male parr were aggressive just prior to spawning, with a decrease in aggression over a broad range of OSRs from 1 to 7.4. Similarly, literature data for three other salmonid species indicated a decrease in aggression with increasing OSRs over a range of 1–6.33. These observations suggest that there is considerable variability in competitive behaviour, even within alternative phenotypes. Because our data are derived from repeated observations on the same individuals of different genetic origin, further confirmation of these findings is desirable. Nevertheless, our study underscores the importance of measuring competitive behaviour and OSR at ecologically relevant spatial and temporal scales, both of which may differ between alternative maturation phenotypes.     

Factors affecting aggressive behaviour of spawning migratory males towards mature male parr in masu salmon Oncorhynchus masou

This study examined whether dominant migratory males (adopting fighter tactics) of the masu salmon Oncorhynchus masou would more aggressively attack large mature male parr (adopting sneaker tactics) as large mature male parr are expected to have the potential to cause a greater decrease in fertilization success. The frequency of aggressive behaviour was not related to the body size of males, and it increased with the frequency of interactions with mature male parr. The fertilization success of mature male parr was much lower than migratory males, and no relationship was observed between fertilization success and aggressive behaviour. The low fertilization success of mature male parr, despite infrequent aggressive behaviour by migratory males, indicates that there might be little benefit for migratory males to attack mature male parr more aggressively according to their body size.     

The relationships between anadromy, sex ratio and parr growth of Arctic charr in a lake in North Norway

Relationships between the degree of anadromy, sex ratio and parr growth of Arctic charr Salvelinus alpinus were investigated in Lake Storvatn in Hammerfest town, by estimating the densities of resident and anadromous charr in the lake, and by comparing the smolt characteristics of fish captured in the outlet river with those of fish of the same age in the lake. About two-thirds of the charr older than 5 years were anadromous. The sex ratio of smolts was approximately 1 : 1 and the frequency of mature male parr in the lake was low. As females tended to dominate the mature portion of the anadromous population, there was probably a relatively higher mortality among sea-run male smolts. The youngest smolts (3+ and 4+) were probably recruited from fast-growing parr in the littoral zone, while older smolts (>4+) may have been recruited from all habitats in the lake.     

Reproductive strategies of Atlantic salmon: ecology and evolution

Atlantic salmon (Salmo solar, Salmonidae) show a diversity of life history, behavioural and morphological adaptations for reproduction which have evolved as an outcome of competition to maximize reproductive success. Reproductive traits of females have been shaped principally by natural selection for offspring production and survival, those of males by sexual selection for access to matings. Female Atlantic salmon invest approximately six times more energy in offspring production (i.e. gonads) than males and face an important trade-off between number and size of eggs to produce that will maximize the number of surviving offspring. Timing of breeding and the construction of nests appear adapted to increase offspring survival. The most important determinant of female breeding success is body size because it affords high fecundity, access to breeding territories and decreased probability of nest destruction. Asynchronous female spawning and the male ability to spawn rapidly and repeatedly results in male-biased operational sex ratios that generate intense male competition for mates. This has likely been responsible for the evolution of elaborate male secondary sexual characters associated with fighting and status signalling. Furthermore, it has given rise, through frequency-dependent selection, to two alternative male breeding phenotypes: (1) large, anadromous males; and (2) small, mature male parr. Anadromous males invest heavily in behavioural activity on the spawning grounds, searching and fighting for mates and courting them, with body size being an important determinant of their breeding success. This behavioural activity carries a heavy cost, as anadromous males have significantly reduced survival relative to females. In contrast, mature male parr invest proportionally more in testes for sperm competition and attempt to sneak access to matings. While this behaviour also carries costs in terms of subsequent growth and survival, male parr are more likely to breed again, either prior to or following a migration to sea, than anadromous males. While knowledge about the breeding of Atlantic salmon is detailed, we are only beginning to understand the ultimate causes and/or functional significances of their reproductive strategies. Predictive models of the life history variation are developing, focusing on the need for empirical study and testing of life history and reproductive patterns.     

Effect of stripping on the length, condition and gonadal state of mature male Atlantic salmon, Salmo salar L., parr during autumn and winter

Hatchery-reared mature male Atlantic salmon parr were shorter than immature parr of the same age through the winter period and this difference increased prior to smolting in spring. Stripping had no effect on growth. In autumn mature male parr had a higher condition factor (CF) than immature parr, but from early January no difference was observed between unstripped mature males and immature parr. Stripping reduced the CF of male parr but the difference had disappeared by the time of smolting when the CFs of both mature groups were lower than that of immature fish. The quantity of expressible milt in stripped males decreased from c . 3% body weight in November and December to <0.05% by 2 March, after which no further milt expression was recorded. Milt expression in previously unstripped males was about 1% of body weight on 2 March, similar to that of stripped males 1 month earlier.     

Relationship between metabolism, sex and reproductive tactics in young Atlantic salmon (Salmo salar L.)

Atlantic salmon can differ markedly in their growth and in the timing of reproductive maturation, leading to the dramatic contrast between the large anadromous adults and the diminutive mature male parr. This study examined the growth rates, anatomical and physiological characteristics of parr during the adoption of their discrete life histories to ascertain whether these properties can explain tactic choice. To minimise the impact of habitat differences upon these attributes, salmon were reared in the laboratory until 1.5years of age, when the "decisions" to undergo smoltification or to mature as parr had been taken. At 1.5years, both males and females showed bimodal size-frequency distributions. Neither the population of origin nor the paternal reproductive tactic influenced the "decision" to mature or the growth trajectories. Growth rate (% massday(-1) during their final 10months) and the % male and female offspring in the upper modal group were strongly correlated and varied markedly among families. Mean growth rate per family was negatively correlated with mean metabolic rate per family at emergence. Growth rate decreased as a function of parr size in January and the growth rates of upper modal fish were displaced upwards relative to those of lower modal fish. Most males in the smaller size mode matured, whereas all other fish began smoltification. Mature male parr did not differ from similarly sized female pre-smolt in routine metabolic rate, but these smaller fish had higher metabolic rates than larger male and female pre-smolts. However, mature parr differed markedly from similarly sized females and from larger male and female pre-smolts in possessing higher oxidative and lower glycolytic capacities in muscle. Overall, these data are consistent with the interpretation that growth rates dictate the distribution of parr between upper and lower modal groups. Individuals from faster growing families would be more likely to pass the threshold for smoltification and to accelerate growth, whereas those from slower growing families would remain in the lower mode. The use of metabolic capacities, e.g. metabolic rate, was linked with modal group, whereas muscle oxidative capacity was linked with male maturity. Mean family metabolic rate at emergence was negatively linked with mean growth during the subsequent year, suggesting that metabolic efficiency facilitates growth and eventually smoltification.     

Peculiarities of sperm production by anadromous and parr Atlantic salmon (Salmo salar L.) and fish cultural characteristics of such sperm

This study describes peculiarities of sperm production by anadromous and precocious parr Atlantic salmon. It was possible to obtain 15 sperm samples with total volume of 130 cm³ from anadromous males at the peak of the spawning run. Changes in the sperm characteristics with the increase of the sea-life age and weight of anadromous males are shown. Such changes are also shown throughout the spawning period. The properties of parr spermatazoa were investigated and it is suggested that these spermatozoa are suitable for insemination.     

Characteristics of mature male parr in the northernmost Atlantic salmon populations

The incidence, relative abundance and biological characteristics of mature male parr of Atlantic salmon Salmo salar were studied in two subarctic (69–70 N°) river systems in the northernmost part of Scandinavia. The proportion of mature males was low (0–25%) among ≥1 year‐old parr, and clearly lower than reported earlier in more southern rivers. The ages of mature males ranged from 1+ to 6 + year, the most abundant age group was 3 + year. Both age structure and size of the mature male parr varied between rivers and years. Mature male parr in the main stem were younger and also smaller than the parr of the same age in the tributaries.     

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.     

Genetic variation in threshold reaction norms for alternative reproductive tactics in male Atlantic salmon, Salmo salar

Alternative reproductive tactics may be a product of adaptive phenotypic plasticity, such that discontinuous variation in life history depends on both the genotype and the environment. Phenotypes that fall below a genetically determined threshold adopt one tactic, while those exceeding the threshold adopt the alternative tactic. We report evidence of genetic variability in maturation thresholds for male Atlantic salmon (Salmo salar) that mature either as large (more than 1 kg) anadromous males or as small (10-150 g) parr. Using a common-garden experimental protocol, we find that the growth rate at which the sneaker parr phenotype is expressed differs among pure- and mixed-population crosses. Maturation thresholds of hybrids were intermediate to those of pure crosses, consistent with the hypothesis that the life-history switch points are heritable. Our work provides evidence, for a vertebrate, that thresholds for alternative reproductive tactics differ genetically among populations and can be modelled as discontinuous reaction norms for age and size at maturity.     

Impact of precocious male parr on the effective size of a wild population of Atlantic salmon

1. There is growing evidence that sexually mature but morphologically juvenile males of Atlantic salmon (precocious or mature male parr) actively participate in reproduction and, therefore, in the genetic composition of the populations of this species. The impact of mature male parr on the effective population size (N_e) of such populations has been previously studied under experimental settings, but no studies have been performed directly on natural populations. 2. Continuous monitoring and sampling of all sea returns is possible in the Lérez River (northwest of Spain). From demographic data on variances of reproductive success and genetic data from six microsatellite marker loci we carried out parentage assignment and assessed the impact of male parr on demographic and genetic estimates of N_e in two consecutive years. 3. Our results reveal that: (i) approximately 60% of the total sire paternity is attributable to mature parr; (ii) mature parr decrease the variance of reproductive success of males by a threefold factor and increase the effective population size of males by a 10‐fold factor; (iii) however, they do not substantially affect the variance of reproductive success and the effective size of females; (iv) mature parr increase two‐to threefold the overall effective size of the population but the ratio N_e/N, where N is the population size including or not mature parr in each case, is not affected.     

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.     

Responses of immature male masu salmon parr to the urine of mature males

Responses of male masu salmon Oncorhynchus masou parr to mature male urine were investigated in a Y-maze trough. Immature masu salmon made fewer entries into the channel conditioned by mature male urine than that with control water. This phenomenon may suggest that immature males avoid sexually active males in the spawning season.