Male Parr Research Articles

Mature male parr contribution to the effective size of an anadromous Atlantic salmon (Salmo salar) population over 30 years

We describe temporal changes in the genetic composition of a small anadromous Atlantic salmon (Salmo salar) population from South Newfoundland, an area where salmon populations are considered threatened (COSEWIC 2010). We examined the genetic variability (13 microsatellite loci) in 869 out-migrating smolt and post-spawning kelt samples, collected from 1985 to 2011 for a total of 22 annual collections and a 30 year span of assigned cohorts. We estimated the annual effective number of breeders (Nb) and the generational effective population size (Ne) through genetic methods and demographically using the adult sex ratio. Comparisons between genetic and demographic estimates show that the adult spawners inadequately explain the observed Ne estimates, suggesting that mature male parr are significantly increasing Nb and Ne over the study period. Spawning as parr appears to be a viable and important strategy in the near absence of adult males.

Contrasting effects of climate change in continental vs. oceanic environments on population persistence and microevolution of Atlantic salmon

Facing climate change (CC), species are prone to multiple modifications in their environment that can lead to extinction, migration or adaptation. Identifying the role and interplay of different potential stressors becomes a key question. Anadromous fishes will be exposed to both river and oceanic habitat changes. For Atlantic salmon, the river water temperature, river flow and oceanic growth conditions appear as three main stressing factors. They could act on population dynamics or as selective forces on life-history pathways. Using an individual-based demo-genetic model, we assessed the effects of these factors (1) to compare risks of extinction resulting from CC in river and ocean, and (2) to assess CC effects on life-history pathways including the evolution of underlying genetic control of phenotypic plasticity. We focused on Atlantic salmon populations from Southern Europe for a time horizon of three decades. We showed that CC in river alone should not lead to extinction of Southern European salmon populations. In contrast, the reduced oceanic growth appeared as a significant threat for population persistence. An increase in river flow amplitude increased the risk of local extinction in synergy with the oceanic effects, but river temperature rise reduced this risk. In terms of life-history modifications, the reduced oceanic growth increased the age of return of individuals through plastic and genetic responses. The river temperature rise increased the proportion of sexually mature parr, but the genetic evolution of the maturation threshold lowered the maturation rate of male parr. This was identified as a case of environmentally driven plastic response that masked an underlying evolutionary response of plasticity going in the opposite direction. We concluded that to counteract oceanic effects, river flow management represented the sole potential force to reduce the extinction probability of Atlantic salmon populations in Southern Europe, although this might not impede changes in migration life history.

Does catch and release affect the mating system and individual reproductive success of wild Atlantic salmon (Salmo salar L.)?

In this study, we documented the breeding system of a wild population of Atlantic salmon (Salmo salar L.) by genetically sampling every returning adult and assessed the determinants of individual fitness. We then quantified the impacts of catch and release (C&R) on mating and reproductive success. Both sexes showed high variance in individual reproductive success, and the estimated standardized variance was higher for males (2.86) than for females (0.73). We found a weak positive relationship between body size and fitness and observed that fitness was positively correlated with the number of mates, especially in males. Mature male parr sired 44% of the analysed offspring. The impact of C&R on the number of offspring was size dependent, as the reproductive success of larger fish was more impaired than smaller ones. Also, there was an interactive negative effect of water temperature and air exposure time on reproductive success of C&R salmon. This study improves our understanding of the complex reproductive biology of the Atlantic salmon and is the first to investigate the impact of C&R on reproductive success. Our study expands the management toolbox of appropriate C&R practices that promote conservation of salmon populations and limit negative impacts on mating and reproductive success.

Mating structure of an endangered population of wild Atlantic salmon (Salmo salar) as determined using sibship reconstruction and a novel method of sex inference

The recent development of molecular genetic markers and methods of inferring relatedness among individuals using multilocus genotype information has allowed new insight into mating systems in the wild. Capitalising on the recently discovered linkage between the microsatellite locus Ssa202 and the sex-determining region of the Atlantic salmon Y chromosome, we developed a novel method to infer the sex of unsampled, wild-spawning parents of some of the few remaining wild, inner Bay of Fundy Atlantic salmon ( Salmo salar ). We inferred that most of the unsampled, reconstructed parents at the half-sib group level were likely polygamous females, while the parents at the full-sib group level (nested within half-sib groups) were likely monogamous males. Given the very low numbers of anadromous salmon returning to inner Bay of Fundy rivers to spawn, the putative male parents were likely mature male parr rather than anadromous males. This suggests that salmonid populations experiencing extreme declines may be composed of a high proportion of related individuals from relatively few sib groups and that mature male parr may provide an important genetic and demographic buffer to population decline.

High marine survival rates of sea‐ranched Atlantic salmon smolts (Salmo salar) that had previously matured as male parr

Abstract The growth and recapture rates of Atlantic salmon, Salmo salar L., smolts that had previously matured as parr were compared with those of immature siblings in a sea‐ranching experiment in western Norway. The smolts were the offspring of three river populations. They were individually tagged, transferred to cages in a small bay where estuarine salinity gradients had been established and released on four dates from mid‐May to early June after either 3 or 7 days of acclimatisation. The previously mature male parr (PMMP) were smaller than their siblings before release, but performed much better during their time in the sea. As grilse, they reached sizes comparable with the formerly immature fish, and their recapture rate was more than four times higher (8.6 vs 2.1%). This difference decreased somewhat during the following years because 0.85% of the immature fish and only 0.1% of PMMP were recaptured as multi‐sea‐winter salmon. The highly successful marine performance of the PMMP demonstrated that this life history strategy may be more flexible than previously believed.

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 1.5 years of age, when the “decisions” to undergo smoltification or to mature as parr had been taken. At 1.5 years, 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 (% mass day − 1 during their final 10 months) 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.

Prior residency advantage for Atlantic salmon in the wild: effects of habitat quality

Prior residency advantages have been explained by an asymmetry between the ‘owner’ and the ‘intruder’ in fighting ability (resource-holding potential) or motivation (value asymmetry (VA)). Here, we tested for the extent of prior residence effects in individually tagged Atlantic salmon juveniles being released in two bouts (4 days apart) during spring along a natural stream, and recaptured 3 months later. A prior residency advantage was detected both in terms of body growth, energy density and male gonad size. As we controlled for effects of initial body size, which correlates with dominance, these findings are in accordance with the VA hypothesis. The growth advantage of first arrivals also increased with local shelter abundance in the stream, which can be expected if a higher resource value of the habitat results in a higher defence motivation. We also found a prior residence effect on spatial distribution, with the second arrivals within each release site being recaptured further downstream. No effect on apparent survival rates was found. The observed reduced growth and energy density may have fitness consequences for the second arrivals, both in terms of lower winter survival rates and later age at maturity. For mature male parr, both decreased body and gonad growth may give an additional disadvantage through reduced fertilization rates during breeding. These costs may help to explain the tendency for stationary behaviour of stream salmonids, as the potential benefits of moving into less crowded areas would be reduced by the risk of becoming an intruder. Prior residence effects may therefore have influenced the evolution of movement behaviour in these organisms.

Reduced daylength stimulates size-dependent precocious maturity in 0+ male Atlantic salmon parr

To study relationships between fish length, photoperiod and the onset of precocious maturity in 0+ parr during intensive rearing of Atlantic salmon (Salmo salar L.), 0+ juveniles of 55–89mm length were individually tagged with Passive Induced Transponders (PITs) in May and exposed to reduced daylength (LD12:12) in May, June or July, or kept as control fish under continuous light (LD24:0). Relationships between the length of the fish and maturity were studied by the use of probabilistic maturation reaction norms. The incidence of mature males and the proportion of fish of lower modal group size in autumn were highest in the groups exposed to short days in May, and lowest under continuous light. In contrast with the expectation that high growth rates promote maturation, the future mature male parr were smaller than the immature males at the start of the experiment, and they also grew more slowly during the subsequent maturation process. Variability in condition factor was low until autumn, when the condition factor of maturing males rose well above that of immature males during autumn as the fish grew from ~80 to ~95mm length. Reduced daylength increased the probability of the onset of precocious maturity in the fish smaller than, but not above a threshold length of ~90–100mm (9 – 11g). Intensively reared parr of 60–90mm, and possibly also smaller fish, may be particularly sensitive to photoperiod manipulations that may influence the probabilities of fish adopting one of the three life-history alternatives, to enter lower or upper mode or to mature precociously.

Effects of habitat on individual reproductive success of mature male parr of Atlantic salmon Salmo salar

The effect of the presence of stone blocks in the spawning habitat on the reproductive success of mature male parr of Atlantic salmon Salmo salar of various sizes and ages was tested in an artificial channel. Shelters allowed smaller individuals to contribute to egg fertilization as much as large parr, suggesting that the size-based dominance observed in a shelterless habitat was not maintained in a more complex habitat.

Reproductive success of Atlantic salmon (Salmo salar) mature male parr in a small river, the Nivelle: influence of shelters

Grimardias D, Merchermek N, Manicki A, Garnier J, Gaudin P, Jarry M, Beall E. Reproductive success of Atlantic salmon (Salmo salar) mature male parr in a small river, the Nivelle: influence of shelters. Ecology of Freshwater Fish 2010: 19: 510–519. © 2010 John Wiley & Sons A/SAbstract – The breeding activity of a small population of Atlantic salmon (Salmo salar L.) was monitored on the Nivelle River in southwest France to estimate the overall contribution of mature male parr and the numbers involved in egg fertilisation. In the twelve redds sampled, 563 eggs were collected for parental assignment and the physical habitat was characterised to investigate the possible relationship between parr reproductive success and habitat complexity. The overall contribution of mature male parr was particularly high (87%, one of the highest estimates ever reported). Concerning habitat complexity, granulometry and shelter diversity were correlated with the number of parr breeders contributing to egg fertilisation in each redd. A complex habitat increased multiple paternity, which could affect the effective size and genetic variability of small salmon populations.

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.

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.

Latitudinal variation in the growth and maturation of masu salmon (Oncorhynchus masou) parr

We examined latitudinal variation in riverine growth and parr maturation of an endemic Asian salmonid, masu salmon ( Oncorhynchus masou ), in 12 rivers located between 36.6°N and 45.4°N. Masu salmon parr showed considerable variation in growth and maturation patterns among populations. Body sizes were generally larger, and parr maturation was common at southern latitudes. Male parr matured at smaller sizes at more southern latitudes. Latitudinal variation in riverine growth and maturation of masu salmon parr was largely attributed to latitudinal changes in temperature and population density. Parr size at age increased with increasing temperature and decreased with population density. Riverine growth conditions were an important environmental factor determining parr maturation for both males and females; however, the occurrence of mature female parr required extremely favorable growth conditions. Water temperature in May, approximately four months before maturation, was the most important environmental factor affecting the maturation of male parr. Our study supports the hypothesis that freshwater residency was promoted by favorable growth conditions at southern latitudes.

Testes and brain gene expression in precocious male and adult maturing Atlantic salmon (Salmo salar).

BackgroundThe male Atlantic salmon generally matures in fresh water upon returning after one or several years at sea. Some fast-growing male parr develop an alternative life strategy where they sexually mature before migrating to the oceans. These so called 'precocious' parr or 'sneakers' can successfully fertilise adult female eggs and so perpetuate their line. We have used a custom-built cDNA microarray to investigate gene expression changes occurring in the salmon gonad and brain associated with precocious maturation. The microarray has been populated with genes selected specifically for involvement in sexual maturation (precocious and adult) and in the parr-smolt transformation.ResultsImmature and mature parr collected from a hatchery-reared stock in January were significantly different in weight, length and condition factor. Changes in brain expression were small - never more than 2-fold on the microarray, and down-regulation of genes was much more pronounced than up-regulation. Significantly changing genes included isotocin, vasotocin, cathepsin D, anamorsin and apolipoprotein E. Much greater changes in expression were seen in the testes. Among those genes in the testis with the most significant changes in expression were anti-Mullerian hormone, collagen 1A, and zinc finger protein (Zic1), which were down-regulated in precocity and apolipoproteins E and C-1, lipoprotein lipase and anti-leukoproteinase precursor which were up-regulated in precocity. Expression changes of several genes were confirmed in individual fish by quantitative PCR and several genes (anti-Mullerian hormone, collagen 1A, beta-globin and guanine nucleotide binding protein (G protein) beta polypeptide 2-like 1 (GNB2L1) were also examined in adult maturing testes. Down-regulation of anti-Mullerian hormone was judged to be greater than 160-fold for precocious males and greater than 230-fold for November adult testes in comparison to July testes by this method. For anti-Mullerian hormone and guanine nucleotide binding protein beta polypeptide 2-like 1 expression changes in precocious males mirrored mature adults (November) but for collagen 1A and beta-globin the pattern was more complex.ConclusionsExpression changes in the fish brain during the process of precocious sexual maturation were small compared to those in the testes. Microarray analysis suggested down-regulation of housekeeping functions and up-regulation of a small number of specific processes. Transcriptional changes in the testes were much more pronounced with anti-Mullerian hormone playing a major role. Expression profiles for mature parr and maturing adult testes indicate subtle differences in gene expression between these two related groups.

Sperm competition between alternative reproductive tactics of the Atlantic salmon in vitro

The maintenance of brood stock in appropriate conditions is an important requirement for the production of high quality offspring. In this study, we investigated fertility of the two life history forms of Atlantic salmon males, precocious parr, brought up in breeding tanks in the hatchery and anadromous, migratory sea-ranched males, caught when returning to the home river. The sperm quality was assessed by experiments between equal amount of sperm from one adult and one parr male in competition to fertilize eggs of a single female. The paternity was determined by a microsatellite analysis. Parr males achieved greater reproductive success than anadromous males under competition, and anadromous adults had greater fertility in controls as compared to the sperm competition situation. In total, parr males achieved 3.6 times greater fertilization success than anadromous males. Sperm ATP content contributed significantly to male fertility. Our results provide evidence that ejaculates of precociously mature Atlantic salmon parr are of increased quality as an adaptation to high sperm competition intensity due to better maintenance in the fish farm than in the wild.

Effects of copper on olfactory‐mediated endocrine responses and reproductive behaviour in mature male brown trout Salmo trutta parr to conspecific females

In the present study, the effects of copper (CuSO4) on the ability of mature male brown trout Salmo trutta parr to detect and react both physiologically and behaviourally to female pheromones were studied. The study was composed of two parts. In the first experiment, priming effects of the female pheromone prostaglandin F2α (PGF2α) were evaluated by determining the amount of milt produced and the blood plasma levels of 11‐ketotestosterone (11‐KT) and 17α,20β‐dihydroxy‐4‐pregnen‐3‐one (17,20β‐P) after the PGF2α exposure. In the second experiment, male parr were placed in a large stream tank together with a group of adult males and ovulated females and their individual behaviours were recorded. In the priming experiment, the amount of expressible milt was significantly lower, less than half, in groups exposed during 4 days to 10 or 100 µg l−1 copper compared with control parr only exposed to water. No significant differences were observed in plasma levels of 11‐KT and 17, 20β‐P. During the behavioural experiment, exposed parr spent less time with the female and had a lower number of courting events. Blood plasma levels of 11‐KT were, however, significantly higher in the group exposed to 100 µg l−1 copper compared with the control group. Furthermore, the exposed group spent significantly less time swimming upstream than did the control group. The present study demonstrates that exposure to copper affects reproductive behaviours and endocrinology of S. trutta male parr.

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

AbstractThe 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.

Hybridization of the Atlantic salmon (Salmo salar L.) and brown trout (S. trutta L.)

Hybrids between the Atlantic salmon and brown trout can be identifi ed on the basis of genes coding for several protein and DNA markers. Hybrids are found in all regions where the Atlantic salmon and brown trout are sympatric. The main causes of the hybridization are the sneaking of mature male parr, escape and release of cultivated fi shes, unstable river discharges, and overfi shing. In numerous experimental crosses, the survival of F1 hybrids varies from zero (a complete loss) to normal. Post-F1 hybridization sometimes results in gynogenesis, hybridogenesis and introgression. The role of hybridization in the evolution of Salmo is discussed.

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

Summary1. 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 (Ne) 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 Ne 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 Ne/N, where N is the population size including or not mature parr in each case, is not affected.

Effects of timing of nest entry and body size on the fertilization success of alternative male reproductive phenotypes of masu salmon (Oncorhynchus masou)

Using a natural population of masu salmon ( Oncorhynchus masou (Brevoort, 1856)) in a stream of Shikaribetsu Lake, Hokkaido, Japan, we combined behavioural observations with genetic parentage analysis to explore the factors affecting fertilization success achieved by alternative mating tactics (fighting by large migratory males and sneaking by small mature male parr). Larger males gained priority access to females; migrant males do this by holding a guarding position near the nesting female and mature male parr do this by adopting sneaker behaviour and attending spawning groups. Status of mature male parr was related to success of nest entry but not to timing of nest entry, although the timing of nest entry influenced fertilization success of sneakers and ejaculation simultaneous with pair spawning was needed for fertilization by sneakers. The relative body size of each male who successfully spawned with a female is also likely to determine the proportion of eggs he fertilized because larger males have larger ejaculate. These results provide insight into factors relating to variation in fertilization success, how body size dimorphisms may be related to fitness, and evolution of alternative mating tactics.